Indian Agricultural
Research Institute, New Delhi.
r. a. r. t. 6.
.\r( a P( S4— n i a r - rn
Annals of Tropical Medicine
AND Parasitology
THE UNIVERSITY OF LIVERPOOL
Annals
OF
Tropical Medicine and
Parasitology
ISSUED BY THE
/iVERPOOL School of Tropical Medicine
Edited by
Professor WARRINGTON YORKK, M.D. M.R.C.P.
Professor IX B. BT.ACKT.OCK, M.IX
Professor W. S. PATTON, M.B.
luiERiTUs Professor R. NEWSTEAD, E.R,S.
VOLUME XXIII
(April 26, 1929, to December 31, 1929)
IJ'ith Frontispiece, eleven plates, seven maps, and one hundred
and tzvelve figures in text
LIVERPOOL :
THE UNIVERSITY PRESS OF TJVERPOOT.
C. Tinling Co., Ltd.
Victoria Street
Liverpool
CONTENTS
No. I. April 26, 1929
PAGE
Adler, S., and Theodor, O.
Attempts to Transmit Leishmania tropica by Bite : the Transmission of
L. tropica by Phlcbolomus sergenti ... ... ... ... ... ... i
Adler, S., and Theodor, O.
Additional Evidence on the Occurrence of L. tropica in wild Phlebotomus
papatasii 19
Sandground, J. H.
Ternidens deminutus (Raillict and Henry) as a Parasite of Man in Southern
Rhodesia ; together with Observations and Experimental Infection
Studies on an Unidentified Nematode Parasite of Man from this Region ... 23
'Paylor, a. W.
Note on the Occurrence of Crithidia in Phlchotomiii mimitin var. Afriennu^ in
Northern Nigeria ... ... ... ... ... ... ... ... 33
Maclean, George.
The Relationship between Economic Development and Rhodesian Sleeping
Sickness in Tanganyika Territory ... ... ... ... ... ... 37
Southwell, T.
Notes on the Anatomy of Stilcsia hcpatlcdy ana on the Genera of the Siib-
Family Thvsauosofninac (including AzdteUininae) ... ... ... ... 47
Stephens, J. W, W.
The Distribution of Blackwatcr Fever in Africa ... ... ... ... 67
Kligler, I. J., and Comaroff, R.
Susceptibility and Resistance to Trypanosome Infections. V. — The Resistance
of Rats to Infection 103
Magath, Thomas B.
The Early Life History of Crepidohothriim testudo (Magath, 1924) 121
Miscellanea 129
V
CONTENTS
No. 2. June 27, 1929
WiTFNBERG, G.
SukUcs on ihc Trcmatode — Family HfUrophyidne
Gray, J. D, Allan.
A Study of Experimental Infection by Treponema duttoni ; with a Review of
the Literature
Adler, S., and Theodor, O.
'I'lie Distribution of Sandflies and Leishmaniasis in Palestine, Syria and
Mesopotamia
Linton, Richard W.
Blood Sugar in Infections with Trypanosoma letoisi
PAGE
131
241
269
307
VI
CONTENTS
No. 3. November 8, 1929
PAGE
Klicler, I. J.
Susceptibility and Resistance to 'rrypanosomc Infection. V'l. — llie Course
of the infection in Splcnectomized Rats 315
Kligler, I. J. ; Geiger, A., and Comaroff, R.
Susceptibility and Resistance to Trypanosome Infections. Vll. — Cause of
Injury and Death in Trypanosome Infected Rats 325
Maclean, George.
Notes on Treatment of Fifty-Two Cases of Rhodesian Trypanosomiasis with
Bayer 205 and Tryparsamide 337
.Maclean, George.
The Action of Prap. 3510 in Rhodesian Sleeping Sickness ... ... ... 345
Nagatv, H. F.
An Account of the Anatomy of Certain Cestodes belonging to the Genera
Stiles id and Avitellina 3^(9
Southwell, T., and Hilmy, I, S. » ■
On a New Species of Phyllohothrium (P. microsomum) from an Indian Shark ... 381
Hilmy, I. S.
Bothriocephalus scorpii (Mueller, 1776) Cooper, 1917 385
Southwell, T., and Hilmy, I. S.
Jardugia paradoxa, a New Genus and Species of Cestodc, with Some Notes on
the Families Acpleidac and Diploposthidie 397
Evans, A. M.
Descriptions of the Early Stages of Two Further Mosquitos Collected in
Southern Nigeria by Mr. L. H. Dunm 407
Evans, A. M.
Notes on Certain Varieties of Anopheles marshaUi I'lieobald
vii
415
CONTENTS
No. 4. December 31, 1929
Huff, Clav G.
The Effects of Selection upon Susceptibility to Bird Malaria in Culex pipiens
Linn, ...
PAGE
427
Mitchell, J. A.
Tunnel Rat-Trap for Stores and Ships 443
Stephens, J.’ W. W.
The Distribution of Blackwaicr Fever in North America 451
Verma, S. C., and DAin:A, M. N.
Acanthoccphala from Northern India. 1 . — A New Genus .Jeanthosentis from
a Calcutta Fish 483
Yorke, Warrington ; Adams, A. R. D., and Murgatroyd, F.
Studies in Chemotherapy. 1 .— IA Method for Maintaining Pathogenic
Trypanosomes alive In Vitro at 37°' C. for 24 Hours 501
Maclean, George.
Stumpy and Posterior-Nuclear Forms in a Strain (Ferox) of Trypanosoma hrucei 519
Evans, A. M.
AHes {Aedimorphus) apicoannulatus Edwards and Yellow Fever : A Correction... 521
Recendanz, Paul.
Pathogenicity of Trypanosoma lewisi and Blood Sugar in Injections with
Trypanosoma lewisi and Bartonella muris ratti ... ... .... ... 523
viii
Professor J. W. W. STEPHENS, F.R.S., retired last September,
after twenty-seven years* service with the Liverpool School of
Tropical Medicine. He was appointed Walter Myers Lecturer in
Tropical Medicine in 1903, and from 1913 to 1928 he occupied
the Alfred Jones Chair of Tropical Medicine. He has been a
member of the editorial staff of this journal from its commencement
in 1907.
Volume XXI 11
April a6, 1929
X ' t
No. r
ANNALS
OF
TROPICAL MEDICINE AND
PARASITOLOGY
ISSUED BY
THE LIVERPOOL SCHOOL OF TROPICAL MEDICINE
Edited by
Professor WARRINGTON YORKE, M.D., M.R.C.P,
Professor D. B, BLACKLOCK, M.D.
Professor W. S. PATTON, M.B.
Emeritus Professor R, NEWSTEAD, F.R.S.
THE INCORPORATED
LIVERPOOL SCHOOL OF TROPICAL MEDICINE
Founded by Sir ALFRED LEWIS JONES, K.C.M.G.
{Affiliated with the Univefsity of Liverpool)
Hon. President : H.R.H. The Duke of York, K.G., G.C.V.O.
Chairman : Sir F. C. Bowring.
Vice-Chainnan : Professor E. W. Hope, O.B.E., D.Sc., M.D.
Hon. Vice-Presidents : The Earl of Derby, K.G., G.C.V.O., C.B., LL.D.
Baron Kylsant, G.C.M.G.
Sir Edward Merewether, K.C.V.O.
Sir H. J. Read, K.C.M.G.
Mr. O. FTarrison Williams
COMMITTEE
Vice-Chancellor H. J. W. Hetherington, |
M.A., LL.D, )
Mr. H. Wade Deacon, C.B.E, [
Associate Professor W. J. Billing I
Professor J. M. Beattie, M.A., M.D., . |
CM., M.R.C.S.. L.R.CP.
ProfessorW. Ramsden, M.A., D.M., B.Ch.l
Mr. Enfield E. Fletcher
Mr. J. N. Sellers
Mr. Cecil Bates
Mr. G. Brocklehurst
Mr. J. R. Danson
Mr. H. D. Dickie
Mr. R. D. Holt
Mr. David Jones
Mr. J. Pickering Jones
Mrs. Percy F. Kipling
Mr. R. Rankin
Mr. J. H. Sharrock
Mr. O. Harrison Williams
Professor W. Yorke, M.D., M.R.C.P.
Professor D. B. Blacklock, M.D,
Professor W. S. Patton, M.B.
University of Liverpool
Council of U niversity of Liverpool
Senate of University of Liverpool
Royal Southern Hospital
Steamship Owners' Association
Shipowners' Association
Mr. J. A. Tinne, M.P., Hon. Treasurer
Mr. J. L. McCarthy, Secretary, C 17 — iS Exchange Buildings, Liverpool
Dr, J. Middlemass Hunt, Hon, Dean, School of Tropical Medicine,
Pembroke Place, Liverpool
Staff, 1929
Alfndyoms Professcr of
Tropical Medicine . . WARRINGTON YORKE, M.D., M.R.C.P.
Dutum Memorial ^Professor of
Entomology .... WALTER SCOTT PATTON, M.B.
Walter Myers Professor of
Parasitology . . . Vacant.
Professor of Tropical Diseases of
Africa .... DONALD BREADALBANE BLACKLOCK, M.D.
Lecturer on Entomology . . ALWEN M. EVANS, M.Sc.
Assistant lecturer on Entomology . Vacant.
Lecturer on Protozoology . . A. R. D. ADAMS, M.D.
Assistant Lecturer in Protozoology . FREDERICK MURGATROYD, M.B.
Lecturer on Helminthology . . T. SOUTHWELL, D.Sc., F.R.S.E.
Clinical Pathologist . . D. UVEDALE OWEN, M.D.
Hon, Lecturer on Clinical
Veterinary Parasitology . . A. W. NOEL FILLERS, F.R.C.V.S.
lecturer on Tropical Surgery . ROBERT ERNEST KELLY, C.B., F.R.C.S.
Lecturer on Tropical Hygiene . A. J. H. RUSSELL, Lieut-Col. I.M.S., C.B.E., M.A., M.D., D.P.H.
Director of Museum • . . ROBERT NEWSTEAD, F.R.S.
Royal Infirmary, LiTerpool
Physician . . . WARRINGTON YORKE, M.D., M.R.C.P.
Assistant Physician • • • Vacant.
Clinical Pathologist . . . D. UVEDALE OWEN, M.D.
Consulting Surgeon • • ROBERT ERNEST KELLY, C.B., F.R.C.S.
The Manaos Research Laboratory
Director HAROLD WOLFERSTAN THOMAS, M.D., C.M.
Sierra Leone Research Laboratory
Director .... DONALD BREADALBANE BLACKLOCK, M.D.
Assistant Direct . . . RUPERT MONTGOMERY GORDON, M.D.
Research Assistants . • . J. FINE, M.B.
MARION WATSON, M.B.
T. H.JDAVEY, M B.
E.'P. HICKS, M B.
VU
THE MARY KINGSLEY MEDAL
This medal was struck in commemoration of the work of the late
Miss Mary Kingsley in West Africa, and is conferred in recognition
of distinguished scientific achievement,
HONORARY RECIPIENTS
Her Royal Highness Princess Christian
Lord Lister *
The Right Hon. Joseph Chamberlain
Prince Auguste d’Arenberg
Mrs. Pinnock
Mr. WiUiam Adamson
Professor William Carter
RECIPIENTS
190S--
Colonel Sir David Bruce, K.C.B.
Geheimrath Professor Robert Koch
Dr, A. Laveran
Sir Patrick Manson, K,C.M.G.
Dr. Griffith Evans
1913—
Professor Fred V. Theobald
i9ir—
1907—
Professor Danielewsky
Dr. Charles Finlay
Mr. W. M. Haffkine
Professor Golgi
Colonel Gorgas
Professor Theobald Smith
1910—
Sir William Macgregor, G.C.M.G.
Professor R. Blanchard
Dr. Anton Breinl
Professor Angelo Celli
Dr. C. W. Daniels
Surgeon-G^n^ral Sir Alfred Keogh
Colonel W, G. King
Professor Nocht
Professor G. H. F. Nut tall
Major Leonard Rogers
Professor J. L. Todd
Surgeon-General Walter Wyman
1919—
Dr. J W. Scott Macfie
The Oswaldo Cruz Institute, Rio de
Janeiro
1920—
Major E. E. Austen, D.S.O. ,,
Dr. A. G. Bagshawe, C.M.G.
Dr. Andrew Balfour, C.B.
Dr. A. L. G. Broden
Mrs. Chalmers, in recognition of the
work of the late Dr. A. J. Chalmers^
Professor B. Grassi , . ^ *
Professor K. T. Leiper
Professor F. Mesnil " '
Dr. Edmond Sergent
Dr. C. W. Stiles
Dr. T. Zammit
vai
THE ALAN H. MILNE MEDAL
This medal was struck to commemorate the late Alan H. Milne,
C.M.G., the first Honorary Secretary of the School (1899-1917), and
is awarded twice yearly on the recommendation of the examiners
for the Diploma in Tropical Medicine.
/P2/— /P26—
George PhiUip Farmer Alien John McPhail Campbell
Triloki Nath Varma
Quinton Stewart 1927 —
Alexander M. Gillespie
1 923 — - Josepli Hector Pollinger
John Cecil Cruickshank Ragade Sanjiva Rao
1924 —
George Maclean
Frederick John Carlyle Johnstone
Bernard Langridge Davis
1925 —
Khwaja Samad Shah
Alfred Robert Davies Adams
Alfred J. Hawe
1928 —
Joseph Fine
1929 —
ian Cameron Middleton
IX
NOTICE
The following courses of instruction are given by the Liverpool
School of Tropical Medicine each year : —
(1) Two courses for the Diploma in Tropical Medicine,
commencing on the ist October and the 7th January.
The D.T.M. examinations are held in December and
March.
(2) Two courses for the Diploma in Tropical Hygiene,
commencing on the 12th January and the 26th April.
The D.T.H. examinations are held in March and July.
(3) Two courses in Veterinary Parasitology, commencing on
1st October and the 7th January.
DIPLOMA IN TROPICAL MEDICINE
This Diploma shall be awarded only to candidates who possess
a qualification to practise Medicine recognised for this purpose by
the University, and who present satisfactory certificates of having
attended approved courses of study, and pass the prescribed
examination.
DIPLOMA IN TROPICAL HYGIENE
This Diploma can only be taken by those who have already
obtained the D.T.M.
* The course for this Diploma will not be conducted unless
at least five applications are received, and no application for
admission can be considered later than December 21st and
March 31st respectively.'
FEES
D.T.M. Course
D.T.H. Course
Course in Veterinary Parasitology
Each Diploma Examination
... Twenty Guineas
... Ten Guineas
... Fifteen Guineas
.... Five Guineas
Fee for use of a School microscope during one term ... One Guinea.
For prospectus and further information, application should be
made to the Hon. Dean, School of Tropical Medicine, University of
Liverpool.
X
The following have obtained the Diploma in Fropical Medicine
of the University of Liverpool : —
Diploma in
Date of
Diploma
1904 Augustine, Henry Joshua
1904 Bennett, Arthur King
1904 Bruce, William James
1904 Byrne, John Scott
1904 Clayton, Thomas Morrison
1904 Dalziel, John McEwen
1904 Dee, Peter
1904 Greenidge, Oliver Campbell
1904 Hehir, Patrick
1904 Khan, Saiduzzafor
1904 Laurie, Robert
1904 Maclurkin, Alfred Robert
1904 McConnell, Robert Ernest
1904 Nicholson, James Edward
1904 Philipson, Nicholas
1904 Sharman, Eric Harding
1904 Thomson, Frank Wyville
1904 Walker, George Francis Clegg
1905 Anderson, Catherine Elmslie
1905 Brown, Alexander
1905 Caldwell, Thomas Cathcart
1905 Critien, Attilio
1905 Hooton, Alfred
1905 Hudson, Charles Tilson
1905 Illington, Edmund Moritz
J905 Macfarlanc, Robert Maxwell
1905 Maddock, Edward Cecil Gordon
1 905 Moore, James Jackson
1905 Nightingale, Samuel Shore
1905 RadcHffe, Percy Alexander Hurst
1905 Young, John Cameron
1906 Adie, Joseph Rosamond
1906 Arnold, Frank Arthur
1906 Bate, John Brabant
1906 Bennetts, Harold Graves
1906 Carter, Robert Markham
1906 Chisholm, James Alexander
1906 Clements, Robert William
1 906 Dundas, James
1906 Faichnie, Norman
1906 Jeffreys, Herbert Castelman
1906 Mackenzie, Donald Francis
1906 Pailthorpe, Mary Elizabeth
1906 Palmer, Harold Thornbury
1906 Pearse, Albert
1906 Sampey, Alexander William
1906 Smithson, Arthur Ernest
1906 Taylor, Joseph van Someron
1906 Taylor, William Irwin
1906 Tynan, Edward Joseph
1906 Watson, Cecil Francis
1906 Willcocki, Roger Durant
1906 Williamson, George Alexander
1907 Allan, Alexander Smith
1907 Allwood, James Aldred
1907 Bond, Ashton
1907 Branch, Stanley
Tropical Medicine
Date of
Diploma
1907 Collinson, Walter Julius
1907 Davey, John Bernard
1907 Donaldson, Anson Scott
1907 Fell, Matthew Henry Gregson
1907 Gann, Thomas William Francis
1907 Grjiham, James Drummond
1907 Hiscock, Robert Carroll
1907 Keane, Joseph Gerald
1907 Kennan, Richard Henry
1907 Kenrick, William Hamilton
1907 Le Fanu, George Ernest Hugh
1907 Mackey, Charles
1907 Maddox, Ralph Henry
1907 McCarthy, John McDonald
1907 Raikes, Cuthbert Taunton
1907 Ryan, Joseph Charles
1907 Vallance, Hugh
1908 Caverhill, Austin Mack
1908 Crawford, Gilbert Stewart
1908 Dalai, Kaikhusroo Rustomji
1908 Dansey-Browning, George
1908 Davidson, James
1908 Dickson, John Rhodes
1908 Dowdall, Arthur Melville
1908 Glover, Henry Joseph
1908 Greaves, Francis Wood
1908 Goodbody, Cecil Maurice
1908 Harrison, James Herbert Hugh
1908 Joshi, Lemuel Lucas
1908 Le Fanu, Cecil Vivian
1908 Lucthgen, Carl Wilhelm Ludwig
1908 Mama, Jamshed Byramji
1908 McCay, Frederick William
1908 McLcllan, Samuel Wilson
1908 Pearce, Charles Ross
1908 Schoorel, Alexander Frederik
1908 Smith, John Maegregor
1908 Stewart, George Edward
1908 Tate, Gerald William
1908 Whyte, Robert
1909 Abercrombie, Rudolph George
1909 Allin, John Richard Percy
1909 Armstrong, Edward Randolph
1909 Barrow, Harold Percy Waller
1909 Beatty, Guy
1909 Carr-White, Percy
1909 Chevallier, Claude Lionel
1909 Clark, William Scott
1909 ^Cope, Ricardo
1909 "Fleming, William
1909 Hantchell, Hother McCormick
1909 Hayward, William Davey
1909 Henry, Sydney Alexander
X909 Innet, Francis Alexander
1909 Jackson, Arthur Frame
X909 Kaka, Sorabji Manekji
1909 McCabe-Dallas, Alfred Alexander Donald
XI
Dautf
•Diplifma
1909 Meldrum, William Percy
1909 Murphy, John CuUinan
1909 Samuel, Mysore Gnananandaraju
1909 Shroff, Kawasjee Byramjee
1909 Thornely, Michael Harris
1909 Turkhud, Violet Ackroyd
1909 Webb, William Spinks
1909 Yen, Fu-Chun
1910 Brabazon, Edward
1910 Castellino, Louis
1910 Caulcrick, James Akilade
1910 Dowden, Richard
1910 Haigh, William Edwin
1910 Hamilton, Henry Fleming
1910 Hefferman, William St. Michael
1910 Hipwell, Abraham
1910 Homer, Jonathan
1910 Houston, William Mitchell
1 910 James, William Robert Wallace
1910 Johnstone, David Patrick
1910 Koske, Vishnu Tatyaji
1910 Macdonald, Angus Graham
1910 Macne, John Wm. Scott
1910 Manuk, Mack Walter
1910 Munson, Cecil Charles
1910 Nanavati, Kishavlal Balabha
1910 Nauss, Ralph Wclty
1910 Oakley, Philip Douglas
1910 Pratt, Ishmael Charles
1910 Sabastian, Thiruchelvam
1910 Shaw, Hugh Thomas
1910 Sieger, Edward Louis
1910 Sousa, Pascal John de
1910 Souza, Antonio Bernardo de
1910 Waterhouse, John Howard
1910 White, Maurice Forbes
191 X Blacklock, Donald Breadalbane
1911 Brown, Frederick Forrest
1 91 1 Chand, Diwan Jai
1911 Holmes, John Morgan
1911 levers, Charles Langley
1911 lies, Charles Cochrane
1 9 1 1 Ingram, Alexander
X911 Kirkwood, Thomas
1911 Knowles, Benjamin
1914 Liddle, George Marcus Berkeley
1911 Lomas, Emanuel Ken worthy
1 9 1 1 Mackarell, William W right
1911 MacKnight, Dimdas Simpson
1911 Mascarenhas, J oseph Victor
1911 Murray, Ronald Roderick
1911 pluwole, Akidiya Ladapo
19x1 Rao, Koka Ahobala
19X I Sinton, John Alexander
1911 Tarapurvalla, Byramji Shavakshah
191 1 Taylor, John Archibald
19x1 Woods, William Medlicott
1912 Aeria, Joseph Reginald
19x2 Anderson, Edmund Litchfield
1912 Borle, James
1912 Bowie, John Tait
1912 Brassey, Laurence Percival
Date of
Diploma
X912 Christie, David
19x2 Dillon, Henry de Courcy
1912 Dunn, Lillie Eleanor
X9X2 Hardwicke, Charles
X912 Jagose, Jamshed Rustomji
19x2 Kochhar, Mela Ram
19x2 McGusty, Victor William Tighe
1912 Milne, Arthur James
X912 Mitra, Manma^a Nath
X912 Myles, Charles Duncan
X912 Pelly, Huntly Nevins
1912 Prasad, Bindeshwari •
X9X2 Prentice, George
X912 Ross, Frank
19x2 Russell, Alexander James Hutchison
1912 Ruthven, Morton Wood
1912 Sandilands, John
1912 Seddon, Harold
1912 Smalley, James
1912 Strickland, Percy Charles Hutchison
X912 Watson, William Russel
19x3 Austin, Charles Miller
X913 Banker, Shiavux Sorabji
X913 Becker, Johann Gerhardus
1913 Carrasco, Milton
19x3 Clark, James McKillican
1913 Forsyth, Charles
X913 Grahame, Malcolm Claude Russell
1913 Grieve, Kelburne King
X913 Hargreaves, Alfred Ridley
1913 Hepper, Evelyn Charles
X913 Hiranand, Pandit
19x3 Jackson, Oswald Egbert
X913 Khaw, Ignatius Oo Kek
X913 MacKelvie, Maxwell
19x3 MacKinnon, John MacPhail
1 9 13 Macmillan, Robert James Alan
X9X3 Mouat-Biggs, Charles Edward Forbes
1913 Noronha, John Carmel
19x3 O’Connor, Edward
X913 Olubomi-Beckley, Emanuel
X913 Pestonji, Ardeshir Behramshah
X9X3 Puttanna, Dodballapur Sivappa
X9X3 Reford, John Hope
19x3 Smith, Edward Arthur
X913 Stewart, Samuel Dudley
X913 Walker, Frederick Dearden
X9X3 Wilbe, Ernest Edward
1913 Wilson, Hubert Francis
19x3 Yin, TJlg Ba
19x3 Y oung, William Alexandex
19x4 Arculli, Hassan el
X914 Chohan, Noormahomed Kasembha
X914 Connell, Harry Bertram
X9X4 Gerrard, Herbert Shaw
1914 Gimi, Hifji Dorabji
X9X4 Gwynne, Joseph Robert
X 9 X 4 Hodkinson, Samuel Paterson
X9X4 Jackson, Arthur Ivan
X9X4 Kaushash, Ram Chander
1914 Kelsall, Charles
-i9i4 Luanco y Cuenca, Maxcimino
X9X4 Mishah, Abdul>Ghani Naguib
Date of
Diploma
1914 Naidu^ Banj^alore Pasupulati Balakrtshna
1914 Rowe, John Joseph Stephen
1914 R07, Raghu Nath
19x4 Shiveshwarkar, Ramchandra Vishnu
1914 Sur, Sachindra Nath
1914 Talati, Dadabhai Cursed ji
1914 Wilkinson, Arthur Geden
19x4 Wright, Ernest Jenner
19x5 Lobo, John Francis
1915 Madhok, Gopal Dass
1915 Pearson, George Ho worth
1915 Swami, Karumuri Virabhadra
1915 Wood, John
X916 Barseghian, Mesroob
1916 Chaliha, Lakshmi Prasad
1916 Lim, Albert Liat Juay
1916 Lim, Harold Liat Hin
19x6 Metzger, George Nathaniel
1916 Sdderstrom, Erik Daniel
1916 Wheeler, Louis
X917 Chapman, Herbert Owen
X917 Krishnamoorthy, Yedatore Venkoba
X917 Lipkin, Isaac Jacob
X918 Watts, Rattan Claud
1919 Bowle-Evans, Charles Harford
1919 Burnie, Robert McColl
19x9 Celestin, Louis Abel
1919 Cummings, Eustace Henry Taylor
19x9 Darling, Georgina Renington
X9X9 Drake, Joan Margaret Fraser
1919 Fraser, William James
1919 Gordon, Rupert Montgomery
X919 Krige, Christian Frederick
X919 Maplestone, Philip Alan
1919 Oluwole, Isaac Ladipo
X919 Rustomjee, Khusshuyee Jamesidjee
1919 Sawers, William Campbell
1919 Thompson, Mary Georgina
19x9 Turner, Gladys Maude
19x9 Young, Charles James
1920 Adler, Saul
X920 Anderson, William Jenkins Webb
1920 Campbell, George
1920 Cobb, Charles Eric
1920 Cobb, Enid Margaret Mary
1920 Connolly, Evelyn Mary
i9:*o Fernandez, Daniel David
1920 Lim, Chong Eang
1920 McHutcheson, George Browne
1920 van der Merwe, Frederick
1920 O' Farrell, Patrick Theodore Joseph
1920 Renner, Edowo Awunor
1920 Vaughan, James Churchwill
1920 Waller, Harold William Leslie
1921 Allen, George Phillip Farmer
1921 Corfield, Charles Russell
1921 Hamid, Abdul
1921 Longhurst, Bell Wilmott
1921 Maevae, George Anthony
1921 Madan, Hans Raj
Z921 MulUgan, William Percival
Date of
Diplomt
X921
1921
X 92 I
X921
X921
1921
1922
1922
1922
1922
X922
1922
1922
1922
1922
1922
1922
1922
1923
1923
1923
1923
1923
1923
1923
1923
1923
1923
1923
1923
*9^3
1923
1924
1924
1924
X924
X924
X924
X924
1924
1924
1924
1924
1924
1924
1924
1924
1924
1924
1924
1925
1925
19^,5
1925
1925
1925
1925
1925
1925
1925
1925
Nixon, Robert
Richmond, Arthur Stanley
Shri Kent, Shamsher Singh
Skinner, James Maegregor
Stewart, Robert Bell
Thomson, Marion
Bhatia, Jagat Ram
Cohen, Morris Joshua
Crawford, Andrew Clemmey
Gilmore, Edward Raymond
Gracias, Cajetan Manuel
Jennings, Arthur Richard
Lethem, William Ashley
Paul, Sachchidananda Hoshen
Finder, John
Rieley, Stanley Desmond
Rutherford, Gladys
Stewart, Quinton
Abelman, B.
Basu, Dhirendranath
Cruickshank, John Cecil
Doherty, Winifred Irene
Edghill, Winifred M.
Elsohn, John
Fraser, N. D.
Lee, R.
Pierce, E. R.
Raja, Rojaporum
Reid, C. B. B.
Richmond, A. E.
Steven, J. B.
White, Charles Francis
Biltmoria, H. S.
Carson, J. C.
Chopra, B. L.
Davis, B. L.
Hardy, M. J.
Jennings, C. B.
Johnstone, F. J. C.
Keirans, J. J.
Lee, S. W. T.
Macdonald, G.
Maclean, G.
Mathur, W. C.
Mitchell, J. M.
Owen, D. Uvedale
Palmer-Jones, Beryl
Sankeralli, E. J.
Singh, H.
Theron, Elizabeth M,
Adams, Alfred Robert Davies
Ashton, Frank Richard
Ashworth, Esther
Bamford, Charles Walker
Beinashowitz, Jack
Black, John
Clark, George
Coghlan, Bernard A.
Collier, Ivy
Crawford, E. J.
Cumming, Patrick Grant
uat 9 aj
Diflama
Date of
Diploma
1925
Ellam, Mary Muriel
1926
Rodrigues, N.
1925
Fifher, Morris
1926
Sachdev, A, P.
1925
Green, Frederick Norman
1926
Singh, B.
1925
Grutu, M. S.
i^z 6
Singh, J.
1925
Hawe, Albert J.
1926
Talib, S. A.
1925
Jafri, Z. H.
1926
Tan, C. L.
* 9*5
Johnstone, Elvy I.
X926
Taylor, Catherine F.
19*5
Kerr, James R.
1926
Turnbull, N. S.
1925
Mackay, Donald M.
X926
Turner, J. G. S.
1925
Mackay, E. K.
1926
Vardya, B. K.
1925
Makkawi, M.
1926
Varma, T. N.
1925
Maldonado, Leopoldo Garcia
1926
Voigt, C.
1925
Mar, Severo Francisco
X926
Wasti, S. N.
1925
* 9*5
Mozoomdar, B. P.
Shah, Khwaja Samad
* 9*7
Allen, C. P.
* 9*5
Skan, Douglas A.
* 9*7
Bahl, M. L.
* 9*5
Stone, Ernest R.
* 9*7
Barrowman, B.
* 9*5
Terrell, C. G.
* 9*7
Bawa, H. S.
* 9*5
Tooth, Frederick
* 9*7
Bilimoria, J. D.
* 9*5
dc Waal, Jacobus Johannes
* 9*7
Burns, W. M.
1926
Aitken, W. J.
* 9*7
* 9*7
Daly, E. J.
Dunlop, G. A.
1926
Ashwbrth, A.
* 9*7
Dyream, V.
1926
Austin, T. A.
1927
Evans, R. R.
1926
Bansikar, R. N.
* 9*7
Farid, M.
1926
Besson, W. W.
* 9*7
Gillespie, A. M.
1926
Bligh-Peacock, R. N.
* 9*7
Gunawardana, S. A.
1926
Bolton, Efiie G.
* 9*7
Harkness, J.
1926
Boodrie, E. H.
* 9*7
Hay, R.
1926
Brito-Mutunayagam, M. A, B,
* 9*7
Hodivala, N. M.
1926
Campbell, J. McP.
* 9*7
Hughes, lEmma
1926
Cullen, T.
* 9*7
Hyslop, Kathleen M.
1926
Davies, H. E.
* 9*7
Ingram-Johnson, R. E.
1926
Dias, B. G. V.
* 9*7
Kapadia, J. S.
1926
Doherty, H. A. A.
* 9*7
Khan, F. A.
1926
Don, E. G.
1927
Khan, M. M.
1926
Earl, J. C. St. G.
* 9*7
Labuschagne, P. N. H.
1926
Fletcher, Beatrice N.
* 9*7
Laird, W. J.
1926
Fowler, H. P.
1927
Lewin, B. F.
1926
Fowler, Isabella J.
* 9*7
Macdonald, J.
1926
Hamilton, J.
* 9*7
McElroy, R. S.
1926
Hodgkinson, Katharine M.
* 9*7
Maclay, W. S.
1926
Jackson, R.
* 9*7
Maguire, H. G.
1926
Kamakaka, K. H.
* 9*7
Mahafly, A. F.
1926
Kennedy, J. H.
* 9*7
Malhotra, A. H.
1926
Khatri, L. D-
* 9*7
Malhotra, A, L.
1926
Lennox, D.
* 9*7
Manghirmalani, B. S.
1926
Lewis, A. J.
* 9*7
Meek, A. I.
1926
^-McConn, C. F.
* 9*7
Mehra, J. N.
1926
Mackay, A. G.
* 9*7
Mehta, H. C.
1926
McLean, N.
* 9*7
Menon, M. V.
1926
MaeSweeney, M.
* 9*7
Miller, H. V. R.
1926
Malhautra, IC L.
* 9*7
Mokand, S. N.
1926
MaUk, S. B.
* 9*7
Murgatroyd, F.
1926
Manuwa, S. L. A.
* 9*7
Murray, A. J.
1926
Merchant, M. E.
* 9*7
Murray, Pauline V,
1926
MitchcU, W. H.
* 9*7
Nevin,- H. M. .
1926
Molony, E. F.
* 9*7
Nirula, P, N.
1926
Nashikkar, S. G*
* 9*7
Olusoga, N. T.
1926
Oppenheimer, F.
* 9*7
Parakh, D. B.
1926
Ormiston, W. S.
* 9*7
Peters, D. O.
1926
Paterson, F. S.
* 9*7
Peters, M. R.
X926
Patterson, F. L.
* 9*7
Pottinger, J. H.
1926
Pouri, V.
* 9*7
Rao, R. S.
1926
Quigley, L. D.
* 9*7
Rodriguez, G. V. S,
1926
Robertson, A.
* 9*7
Shah, S. R. A.
XIV
Dat*^
Diploma
1927 Smgh, H.
1927 Southward, J. F.
1927 Sturton, S. D,
1927 Thompson, Frances C.
1927 dc \^mers, B. J. van de S.
1927 Walkinshaw, R.
1927 Wilkinson, S. A.
1928 Ahluwalia, C. L.
1928 Aidin, A. R.
1928 Anand, J. S.
1928 Askari, S. W. H.
1928 Beveridge, Ruby S.
1928 Biswas, M. K.
1928 Blakemore, W. L.
1928 Camps-Campins, J. M.
1928 Cha(»o, M. O.
1928 Chopra, A. N.
1928 Chaudhuri, J. P.
1928 Choudari, K. V. R.
1928 Cranage, Margaret
1928 Dhala, C. H.
1928 Dhar, K. K.
1928 Dikshit, H. K.
1928 Everard, N. J.
1928 Fine, J.
1928 Ghei, A. N.
1928 Halawani, A.
1928 Henshaw, L. £. R.
1928 Hilmy, I. S.
1928 Holmes, W. £.
1928 Hope-Gill, C. W.
1928 Kane, F.
1928 Kadal, C. L.
1928 Khan, F. M.
1928 Krishna, R.
1928 Lawrence, H. S.
1928 Lawrence, M. R.
1928 McLaren, D. W.
1928 Malhotra, B. D.
1928 Mallick, B. D.
1928 Mason, Jean R.
1928 Menon, E. S. R.
1928 Milne, J.
Date of
Diploma
1928 Mitchell, A,
1928 Mone, R. V.
1928 Morlcy, A. H.
1928 Mostert, H. van R.
1928 Mufty, S.
1928 van Nickerk, S. V.
1928 Pandit, M. K.
1928 Pearce, W. T. A.
1928 Plum, D.
1928 Rao, B. D.
1928 Reid, A.
1928 Sanderson, I.
1928 Setna, H. M.
1928 Shearer, G.
1928 Singh, B.
1928 Sivalingam, S.
1928 Stratton, Ella M.
1928 Suri, R.
1928 Tuli, R. L.
1928 Udvadia, F. F.
1928 Wagle, P. M.
1928 Wahid, A.
1928 Wall-Mesham, Nellie
1928 Whig, P. L.
1929 Chakravarti, K. R.
1929 Crawford, J.
1929 Dale, W. C.
1929 Dogra, J. R.
1929 Drury, G. D.
1929 Gill, T. S.
1929 llerbertson, Margaret A. L.
1929 Innes, J. A. L.
1929 McGregor, J. A.
1929 McQueen, W. B.
1929 Majumdar, B. K.
1929 Middleton, I. C.
1929 Pearse, J. T. F.
1929 Ramdeholl, C.
1929 Robinson, Elizabeth J.
1929 Robinson, P. B.
1929 Shafi, A.
1929 Verghese, T.
1929 Wilson, S. P.
The following have obtained the Diploma in Tropical Hygiene
of the University of Liverpool : —
Diploma in Tropical Hygiene
Date of
Diploma
1926
Aitken, W. J.
Date of
Diploma
1926
MacSweency, M.
1926
Bligh-Peacock, N.
1926
Oppenheimer, F.
1926
Clark, G.
1926
Skan, D. A.
1926
Collier, Ivy
1926
Talib, S. A.
1926
Cullen, T.
1926
Tjumbull, N. S.
1926
1926
Davis, B. L.
Don, E. G. A.
1927
Allen, C. P.
1926
Fowler, H. P.
1927
Austin, T. A.
1926
Hawj!, A. J.
1927
Besson, W. W.
I 92 <^
Lennox, D.
1927
Dunlop, G. A.
1926
Mackay, A. G.
1927
Earl, J. C. St. G.
Han^ton, J.
1926
Mackay, D. M.
1927
1926
McLean, N.
1927
Harkness, J.
XV
Date of
Diploma
Date of
Diploma
1927
Hay, R.
1928
Evans, R. R.
1927
Hyslop, Kathleen M.
1928
Holmes, W. E.
1927
Labuschagne, P. N. H.
1928
Laird, W. F.
McCon, C. F.
1928
Maclay, W. S.
1927
Macdonald, J.
1928
Miller, H. V. R.
1927
Mitchell, Winifred H.
1928
Motley, A. H.
1927
Murray, A. J.
1928
Pearson, G. H.
1927
Ncvin, H. M.
1928
Pottinger, J. H.
1927
Nixon, R.
1928
Sanderson, 1.
1927
Ormiston, W. S.
1928
Sivalingam, S.
1927
Robertson, A.
1928
Wilkinson, S. A.
1927
Walkingahaw, R.
1928
Bilimoria, J. D.
1929
1929
Askari, S. W. H.
Halawani, A.
1928
Blakemore, W. L.
1929
Ailmy, I. S.
1928
Choudari, K. V. R.
1929
Lawrence, H. S.
1928
Dhar, K. K.
1929
Setna, H. M.
ANNALS OF TROPICAL MEDICINE
AND PARASITOLOGY
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the paper, and arranged in the following way : —
Robinson, S. (1914). The spleen in malaria. Ann. of Nosology,
20 , 20-25.
Smith, J. (1900), Enlargement of the, spleen in malaria. Jl. of
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should also be addressed.
XVI
ATTEMPTS TO TRANSMIT LEISHMANIA
TROPICA BY BITE : THE TRANSMISSION
OF L. TROPICA BY PHLEBOTOMUS
SERGENTI
BY
S. ADLER,
AND
O. THEODOR, Ph.D.
[Microbiological Institute, Hebrew University, Jerusalem)
[Received for publication ly January, 1929)
Plate I
In previous papers (1925 and 1926) it was shown that Leishmania
tropica is a natural parasite of Phlebotomus papatasii, and that the
flagellates naturally occurring in this sandfly produce oriental sore
when inoculated into man. It was also shown that L. tropica
ingested from human lesions ex-flagellates in P. papatasii and,
after undergoing a cycle, produces forms which are infective for
man (1926 and 1927). It was further shown (1927) that P, papatasii
can be infected with different species of Leishmania by feeding on
cultures through a membrane, and that L. tropica from cultures
behaves exactly as L. tropica ingested from an oriental sore. As
L. tropica adopts an anterior position in P. papatasii, it was concluded
that transmission in nature takes place by the bite of the sandfly.
It was, therefore, determined to infect sandflies with L. tropica by
feeding on cultures through a membrane and to attempt transmission
by bite on as large a number of volunteers as could be obtained, in
order to eliminate possible negative results due to individual
immunity. That a complete immunity to L. tropica, in the form of
L.D. bodies from a human lesion exists, is shown by the
following experiment, previously recorded in this journal (1926).
Material from an experimental human lesion (a subcutaneous
nodule) was inoculated into two human beings (20.4.26). One
has remained negative up to date, and the other devdoped an oriental
I
2
sore from which L. tropica was cultured (Strain F), The strain
obtained from this case was used for infecting sandflies and
attempting to infect human beings by bite.
That there is immunity in man to the flagellates of L. tropica
from artificially infected sandflies is shown by the following facts,
also previously recorded in this journal (1927). Out of nineteen
volunteers inoculated with L. tropica after a development of eight
to twenty-one days in the sandfly, six developed oriental sore.
The thirteen other volunteers are still negative.
It is also shown (1927) that cultures of L. tropica on Locke-Serum-
Agar lose their infectivity for man, but that infectivity is restored
if the culture is passed through a sandfly. It was, therefore, expected
that a positive result would eventually be obtained by feeding the
sandflies infected with cultures on human beings.
A strain of L. Tropica isolated on 11.8.27, from the above-
mentioned case, was employed (Strain F). This strain was used
because of its great infectivity for P, papatasii. Strains of L. tropica
vary greatly in their infectivity for P. papatasiiy and this may
explain some puzzling facts in the epidemiology of oriental sore,
e.g., in Jericho, where P. papatasii is more numerous than in any
part of the Middle East we have examined, and, where imported cases
are few or none, a few cases of oriental sore occur annually, but the
large majority of the population escape the disease. In Bar Elias,
a village in Syria, P. papatasii and P. major are the only sandflies
present which bite man, but P. major is rare and P. papatasii is
abundant. During the last six years almost every person in the
village has become infected with oriental sore and, accepting the
sandfly theory of Leishmaniasis, the only vector to be considered is
P. papatasii. In Bar Elias we are dealing with a strain which is
highly infective for P. papatasii^ much more so than the strain from
Jericho. We hope to discuss this point more fully in a future
communication.
A total of 750 laboratory bred sandflies were fed on emulsions
varying from 100 to 6,000 per cmm., and of these 708 sandflies became
infected. In nine experiments, 124 sandflies were fed on emulsions of
from less than 100 up to 500 flagellates per cmm. (i.e., 10 to 50
flagellates per feed), 91 became infected. In two of these
experiments nearly all the sandflies were infected (19 out of ao).
3
In addition, 69 sandflies fed on emulsions of L.D. bodies, in
inactivated normal blood, from selected cultures in medium made
up with immune serum, and 26 became infected. There was no
difference in the infection rate between emulsions made up with
normal and immune serum.
There is evidence that blood is inactivated almost immediately
in the sandfly. This evidence rests on the following grounds.
Normal blood, both of man and of the rabbit, is strongly lytic for
L. tropica, L. donovani and L, infantum. This lytic action depends
entirely on complement, and disappears on inactivation. Re-feeding
infected sandflies on fresh blood makes no difference to the infection
rate and, in the majority of cases, does not influence the intensity of
the infection in the sandfly. If sandflies are allowed to feed on an
emulsion of L, tropica in active blood, where the flagellates are
rapidly disintegrating a high infection rate is, nevertheless, produced
in the sandflies, proving that the lytic action ceases at once inside
the sandfly.
E.g. 18.9,27. An emulsion of L. tropica in active rabbit blood
was made up to 20,000 cmm. Twelve sandflies fed on this emulsion.
After one and a half hours, when all the sandflies had fed, the emulsion
was reduced to less than 300 per cmm. Nine of the sandflies were
subsequently found positive.
22.9.27. An emulsion of L. tropica in active rabbit serum
coloured with inactivated blood was made up to 2,000 per cmm.
After half an hour the emulsion was too poor to be counted in a
haemocytometer (less than 200 per cmm.) ; 45 sandflies fed on this
emulsion half an hour after it was made up. Of these, 19 were
subsequently found positive, proving that the lytic action of
the serum ceased inside the sandfly.
Because of the high infectivity of the strain of L, tropica used,
the above experiments are not as conclusive as the following
one.
18.9.27. An emulsion of a culture of visceral Leishmania from a
dog in active rabbit blood was made up to 6,000 per cmm. ; 37
sandflies fed on this emulsion. The majority fed within
half an hour after the emulsion was made up. The emulsion was
found to be reduced to less than 300 per cmm. ; 7 sandflies were
subsequently found positive. Had the lysis continued inside the
4
sandflies as it did in the emulsion, the infection rate would have
been almost nil.
Occasionally one finds a rabbit serum which contains heat stable
lysins not destroyed by inactivation or by heating to 75® C. for
half an hour. Experiments similar to those above showed that the
heat stable lysins are also inactive inside the sandflies.
Table I shows the number of positive sandflies (infected from
Strain F) fed on each volunteer, the number of days after the
infecting feed on culture, and the period during which the feeds took
place.
It will be seen from the table that there was a .total of 253 feeds
by sandflies (P. papatasii) subsequently found positive. As most
of the sandflies bit from two to five times before completing their
feed, there was a total of over 500 bites. Of the 253 feeds, 54 were
from six to seven days, 169 from eight to fifteen days, and 30 from
sixteen to thirty days after the infecting feed. The sandflies were
kept at temperatures of 19® C. to 23® C., and were re-fed at intervals
of three days.
In a few cases they were re-fed at intervals of two days. -The
longest time a positive sandfly, P. papatasii, lived was 32- days
after the first feed.
Experiment on Volunteer No. 8, with P. sergenti.
P. sergenti, No. 122. Hatched in laboratory. Fed on case of
oriental sore from Artuf, 29.7.28.
4.8.28. Bit volunteer No. 8 on the right forearm, but did not
4 raw blood. There was a local reaction which lasted three days.
Sandflies died two hours after biting. The cardia and the
stomach were found heavily infected.
Result : Negative up to date.
The result of the feeding experiments with P. papatasii were
negative in the case of volunteers i, 3 to 12, and the puppy
(volunteers i, 2 and^ W also used for inoculation experiments).
Experiments on Volunteer No. 1.
Sandfly No. 3606. Hatched in laboratory, 16.11.27.
culture eleven days old, cite. 200 'per cmm. Re-fed 21.11.27. Died
and dissected 29.11.27. Heavy infection from stomach up to
5
Table 1.
Showing experiments with infected P. papatasn.
Days after
Number of positive sandflies fed on volunteers
Puppy
Total
number of
infection feed
No. No. No. No.
1234
i
No. No. No. No. No. No. , No. No.
5 6 7 8 9 10 II 12
sandflies
fed on
each day
6
! -
! j ^
31
7
18
3 2
23
8
12 ... 2
8 2Q
42
9
2 5
3 •••
22
10
9 I ... 2
4 4 I
21
11
23-2
3 5 3
18
12
5 3
2 3 J 3 3
4
24
13
4
3 4 - 1 2 I ...
14
14
4 2 ... I
4 . 3
I 3
2 2 ... 3 I
I
’3
16 I
^ ■ -
3
17
I ... I
2 ... 1
5
18
2 ... I 1
I
5
>9
2
I 2
5
20 :
1 - 3
4
21 i
I
2
22 1
2
2
H
I
I
2O
I
...
I
I
I
-
I
.
Total Number
of Sandflies
fed on each
V’olunteer
88 15 2 II
1
19 21 3 ' 67 7 4 7 2
7
253
Period During which Experiments were Performed.
On Volunteer No. i. 3.9.2710 8.3.28. On Volunteer No. 8. 11.12.27 to 26.2.28.
On Volunteer No. 2. 25.9.27 to 8.1.28. On Volunteer No. 9. 3.1.2810 13.1.28.
On Volunteer No. 3. 29.11.27. On Volunteer No. 10. 6.12.2710 8.12.27.
On Volunteer No. 4. 19.12.27 to 13.2.28. * On Volunteer No. ii. 10.1.28 to 15.1.28.
On Volunteer No. 5. 21.10.27 to 28.10.27. On Volunteer No. 12. 3.1.28.
On Volunteer No. 6. 31.10.27 to 12.2.28. On the Puppy. 14.11. 27 to 30.11.27.
On Volunteer No. 7. 5.1.28 to 31.1.28,
6
middle of the proboscis. Part of the flagellates inoculated into
Volunteer No. i, on left forearm.
Sandfly No. 3607. Details as above. Part of flagellates
inoculated into the same scarification as No. 3606.
Result : Negative during observation period of thirteen months.
A sandfly, P. sergenti caught in Baghdad, 27.5.28. Died and
dissected 28.5.28. Heavy infection with flagellates found in stomach
and cardia.
Flagellates inoculated into two points in the left forearm of
Volunteer No. i.
Result : Negative during an observation period of seven months.
Experiment on Volunteer No. 6.
P, sergenti $, No. 106. Laboratory bred. Hatched 27.7.28.
Fed on case of oriental sore from Artuf, 27.7.28. Re-fed on guinea-
pig, 31.7.28., found dead on morning of 4.8.28. Dissected and found
heavily infected. Inoculated on two points on arm of Volunteer
No. 6.
Result : Negative up to date.
Experiments on Volunteer No. 2.
The infected P, papatasii were fed on the upper and external
part of the left forearm and on an area several inches square, about
the middle of the left arm. These feeding experiments were carried
out between 25.9.27 and 8.1.28.
On the nth of November, 1928 (ten months after the last feed by
infected sandflies) this volunteer noted two small lesions on the
left arm on the site on which infected sandflies had fed. These
lesions were examined on 12. 11.28, and found to consist of two minute
vesicles unlike any oriental sore previously examined. Of the
eleven experimental lesions which we have previously recorded, ten
commenced as scaly papules, and one as a subcutaneous nodule.
As the lesions occurred on a site on which sandflies had fed, they
were opened, and smears were made and stained with Giemsa. The
vesicles were found to contain a clear fluid full of extra-cellular L.D.
bodies. On the 13th two more vesicles appeared in the neigh-
bourhood of the first ones. These were examined on the 14th, and
one was found positive.
107 sandflies, P. papatasii, laboratory bred, fed on this case and
7
all were subsequently found negative. Only about a third of the
sandflies fed directly on the lesion, and the remainder fed in the
neighbourhood of the lesions.
It seemed certain that these lesions were caused by flagellates
of L, tropica introduced into the skin by the bites of one or more
of the infected sandflies, but a slight element of doubt appeared.
It was found that during the summer of 1928 Volunteer No. i
lived in the Bokharian quarter of Jerusalem, a quarter where there are
always a number of imported cases of oriental sore from Baghdad,
Aleppo and Persia and where, moreover, sandflies are very common.
Although the lesions appeared on the site on which artificially
infected sandflies had fed, nevertheless the possibility of the lesions
being natural ones must be considered, particularly as several
locally acquired cases of oriental sore have been noted in Jerusalem, in
1928. The experiment cannot, therefore, be regarded as an
absolutely conclusive proof of the transmission of oriental sore by the
bite of P. papatasii.
Other Inoculation Experiments on the Same Volunteer.
Experiment No. i. 23.7,28. Culture material of L. tropica was
inoculated into the tails of four mice, by the method recommended
by Parrot and Donation (1927), who demonstrated that mice are
very sensitive to this method of inoculation with L. tropica. The
same strain was inoculated into two points on the lower part of the
left arm of Volunteer No. 2.
Result : Volunteer No. 2 has remained negative on the site of
the inoculated points within an observation period of five months.
Two mice were found positive on the inoculated sites after ten days.
(Further experiment showed that mice inoculated by this method
show L.D. bodies on the inoculated sites as early as five days after
inoculation.)
Experiment No. 2. 2.8.28. P. sergenti 9, hatched in laboratory
on 27.7.28. Fed on the same day on case of oriental sore from
Artuf. Sandfly kept at 27® C. Died and dissected 2.8.28.
Flagellates from the mid-gut were inoculated into three scarified
points on the right arm of Volunteer No. 2.
Result : On 23.11.28 a raised spot was noted on the site of one of
the scarifications. On examination, L.D. bodies were found.
8
Experiment No. 3. P. sergenti, No. 232. Hatched in laboratory,
7.8.28. Fed, 8.8.28, on case of oriental sore. Re-fed 12,8.28.
16.8.28. Refused to feed. Died and dissected. Was found to be
heavily infected. Flagellates inoculated into two points on the left
deltoid region.
Result : Negative up to date.
The lesion on the right arm appearing actually on the scar of a
previous inoculation with flagellates from an artificially infected
P. sergenti, proves that after six days at 27° C. L. tropica in P. sergenti
is infective for man. In this case the possibility of natural infection
is negligible for, whereas sandflies might feed on a site several inches
square, it is improbable that a wild infected sandfly should feed on
a single experimental point. In the case of P. papatasii it was
shown that L. tropica becomes infective for man after eight days at
19 to 23° C.
THE BEHAVIOUR OF L, TROPICA IN P. SERGENTI
Sinton (1925) first suggested P. sergenti as a possible vector
of oriental sore, after studying the distribution of the sandfly and
the disease. Evidence obtained by a study of distribution of
sandflies must be interpreted very cautiously. Oriental sore is absent
in places where both P. papatasii and P. sergenti occur. We will
deal with the distribution of sandflies and oriental sore in another
communication. For the present we will confine ourselves to
experimental facts obtained by feeding P. sergenti on cultures of
Z. tropica and on oriental sore.
, P. sergenti does not feed readily through membranes and under
laboratory conditions we were not very successful in feeding this
sandfly on man. Only a small proportion, varying from none to
25 per cent, of laboratory bred P. sergenti were induced to feed on
man and, working in Baghdad, we never succeeded in feeding wild
P. sergenti on man although, in nature, these sandflies feed mainly
on human beings. It was noted that P. sergenti feeds more readily
on injured than on normal skin, while P. papatasii shows no selection
and feeds equally well on both normal and injured skin. For the
purpose of breeding P. sergenti we were compdled to leave sandflies
all day in a cage containing a guinea-pig, and even then not more than
about 10 per cent, of the sandflies fed. Fortunately, P. sergenti
9
lays eggs after one feed. Out of over 200 P. sergenti offered a feed
on normal human skin, only five fed, whereas 25 out of 200 fed on
oriental sores.
Owing to the kindness of Dr. A. E. Mills we were able to carry
out the following experiments in the Central Laboratory, Baghdad.
Table II.
Experiments with membranes.
Sandfly
Date
of
feed
Number of
flagellates
per feed
Died
Species
Result
No. I
19.5.28
20 circ.
22.5.28
P. sergenti
Heavy infection in stomach.
No. 2
19.5.28
20 circ.
22.5.28
P. sergenti
Slight infection in cardia.
No. 3
19.5.28
20 circ.
20.5.28
P. papatasii
Negative.
Nos. 4-10
19.5.28
20 circ.
22.5.28
P. papatasii
Heavy infections in stomach.
No. II
20.5.28
20 circ.
22.5.28
P. sergenti
Negative.
No. 12
20.5.28
20 circ.
1
24.5.28
P. sergenti
Heavy infection in stomach.
Slight infection in cardia.
No. 13
20.5.28
20 circ. j
24.5.28
P. sergenti
Slight infection only in cardia.
No. 14
20.5.28
20 circ.
24.5.28
P. sergenti
Negative.
The sandflies were all caught in Baghdad. They were kept
at 30° C.
The experiments, though, few, are conclusive. They show that
L. tropica once established in P. sergenti tends to the anterior position
even if the infection produced in the sandfly is very slight. P. sergenti
is, therefore, a probable carrier of oriental sore.
THE INFECTION OF P. SERGENTI ON ORIENTAL SORE
The sandflies used in the following experiments were laboratory
bred from eggs laid by wild sandflies caught in Baghdad. They
were infected in Mosul on a case of locally acquired oriental sore, and
were subsequently transported to Baghdad, where they were
examined. During six of the eighteen hours' trip to Baghdad, they
were subjected to a temperature of about 40° C. in an open car.
The sandflies were kept in tubes encased in moistened lint. As will
be seen from the following table, the high temperature during
six hours had no deleterious effect on the development of L. tropica.
lO
Table III.
Feeding Experiments with P. sergenti on oriental sore in Mosul.
Sandfly
Hatched
Fed
Died
Results
No. I
2.7.28
4.7.28
7.7.28
Cardia and stomach heavily infected, attachment of
medium and long forms to cardiac valve.
No. 2
2.7.28
4.7-28
7.7.28
Cardia and stomach heavily infected, attachment of
medium and long forms to cardiac valve.
No. 3
3.7.28
5.7.28
7.7.28
Heavy infection in stomach, long forms.
No. 4
3.7.28
5.7.28
7.7.28
Slight infection in stomach.
No. 5
3.7.28
5.7.28
7.7.28
Heavy infection in stomach.
No. 6
, 3 - 7-28
5.7.28
7.7.28
Many ex-flagellating forms in stomach, mostly
medium and short forms.
No. 7
3.7.28
5.7.28
7.7.28
Many ex-flagellating forms in stomach, mostly
medium and short forms.
No. 8
3.7.28
5.7.28
00
Negative.
No. 9
5.7.28
6.7.28 ‘
7.7.28
£x-flagcllating forms in stomach.
No. lo
5.7.28
6.7.28
7.7.28
Negative,
No. II
5.7.28
6.7.28
00
Negative.
No. 12
5.7.28
6.7.28
7.7.28
L.D. bodies and ex-flagellating forms in stomach.
No. 13
3.7.28
4,7.28
8.7.28
Negative contaminated.
No. 14
3.7.28
4.7.28
8.7.28
Heavy infection in cardia, stomach and hind-gut.
Long forms.
No. 15
3.7.28
5.7.28
8.7.28
Heavy infection in stomach and cardia. Long forms.
No. 16
3.7.28
6.7.28
9.7.28
Negative.
Nd. 17
3.7.28
6.7.28
9.7.28
Negative.
It win be seen from the above table that L, tropica ex-flagellates
and multiplies rapidly in P. sergenti. It ascends the cardia within
three days. Of seventeen P, sergenti^ eleven became infected and, of
two P. papatasii fed on the same sore, one was found infected.
Laboratory bred P. papatasii and P. sergenti were fed on two
cases of oriental sore from Dr. A. Dostrowsky's Clinic at the
Rothschild Ho.spital, Jerusalem.
Case I was acquired in Baghdad and was, therefore, transmitted by
P. sergenti or by P. papatasii.
II
Case II was acquired at Artuf, in Palestine, where P, papatasii
is very common, and P. sergenti has never been found. Between
every series of feeds* Case II had an injection of Stibosan. Smears
were taken at regular intervals, and it was found that the parasites
progressively diminished. It will be seen from Table IV that between
27.7.28 (when L.D. bodies in the lesion were very numerous) and
8.8.28, the infection rate in P. papatasii diminished markedly, while
that of P. sergenti was hardly affected. It is, therefore, obvious that
P. sergenti is a more suitable host for the development of the strain
of L. tropica from Case II then even P. papatasii, though the organism
behaves similarly in both sandflies. In three out of eight specimens
of P. sergenti, which died six days after the infecting feed, flagellates
were found in the proximal two-thirds of the proboscis. Out of
sixteen specimens of P. papatasii which died six days and more after
the infecting feed, the proboscis was found infected only in two cases.
In one case, in addition to the anterior infection, flagellates were
found attached in the hind-gut of P. sergenti and the rectum was
also heavily infected.
Table IV.
Experiments with P. papatasii and P, sergenti on oriental sores.
Case
Date of feed
Number of
P. sergenti
fed
Number
positive
Number of
P. papatasii
fed
Number
positive
I.
22.7.28
*
>
30
■
I.
25.7.28
0
0
35
1
I.
27.7.28
0
0
2
0
II.
27.7.28
9
5
23
10
II.
29.7.28
3
3
16
4
II.
1.8.28
0
0
36
5
II.
5.8.28
3
I
35
3
II.
8.8.28
6
4
4*
3
II.
12.8.28
3
I
33
6
II.
15.8.28
0
0
34
4
Total
^5
15
1
285
37
The sandflies were kept at a temperature of 77® C.
12
These observations cannot be generalised for all strains of
L, tropica, because strains vary enormously in their infectivity for
P. papatasii. It is probable that they also vary in their infectivity
for P. sergmti. As an example of the variation in the infectivity of
strains of L, tropica for P. papatasii, the following records will be
sufficient.
Strain from Tunis. This strain was presented by Professor
Nicolle, Director of the Pasteur Institute, Tunis.
Table V.
Behaviour of the strain of L. tropica from I'unis in P. papatasii.
1
Date '
of
experiment
Age
of
culture
Flagellates
per
0*1 cmm.
Number
of
sandflies
fed
Number
positive
Remarks
CO
Days
*4
80
22
19
i Dissected 4 to 8 days after in-
fecting feed.
oo
5
1,000
5
5
Dissected after 4 to 5 days.
18.1.28
8
1,000
10
8
Dissected after 2 to 6 days.
23.8.28
7
600
30
28
Dissected after 4 to 8 days:
Strain of L. tropica isolated from oriental sore in Baghdad.
Table VI.
Behaviour of the strain of L. tropica from Baghdad in P. papatasii.
Date
of
experiment
Age
of
culture
Flagellates
per
O' I cmm.
Number
of
sandflies
fed
Number
positive
Remarks
27.7.28
Days
8
50
H
0
Dissected 4 to 5 days after in-
fecting feed.
29.7.28
10
80
25
2
Dissected after 4 to 6 days very
slight infections.
5.8.28
7
1,000
9
4
Dissected after 4 to 9 days.
7.8.28
6
250
ig
0
—
9.8.28
250
20
0
—
13
The strain of L. tropica isolated from a lesion on the left arm of
Volunteer No. 2 was also only very slightly infective for sandflies.
This strain showed an additional peculiarity in that it tended to
die out in the sandfly, e.g. : — ^3.12.28. 27 sandflies fed on an
emulsion of 1,600 flagellates per o*i cmm. from a culture
nineteen days old. Of 8 sandflies dissected within three days
after the infecting feed, 6 were found positive. Of 19 sandflies
dissected from four to ten days after the infecting feed, only
2 were found positive.
It is necessary to inquire why the results of feeding experiments
with so many heavily infected sandflies gave negative results.
We think that the reason is that at a temperature of 19 to 23° C., only
a small proportion of sandflies acquire an infection in the proboscis.
The pharynx is often completely choked and from here flagellates
enter the buccal cavity. The posterior part of the buccal cavity
may also be plugged with flagellates but, unlike P. argentipes infected
with L. donovani, the whole buccal cavity does not, as far as our
observations go, become completely choked. (We have seen complete
blocking of the buccal cavity of P. papatasii only in one instance.
The sandfly was infected from culture of a strain of L. infantum.)
Flagellates dribble down from the buccal cavity into the proboscis
and they may pass almost up to the tip of the proboscis. Sections
of some heavily infected sandflies showed flagellates in the coelom
and muscle spaces throughout the body and appendages, but not
inside the ova. This condition appears to be without significance
with regard to transmission. It is not known for how long an
insect is viable in this state ; the condition is possibly produced
shortly before death or during the process of dying. We found
later that at higher temperatures (27 to 30° C.) proboscis infections
in P. papatasii are much commoner but, in the experiments recorded
above, the sandflies were kept at 19 to 23® C. This is the probable
reason for so many failures in our attempts to transmit by bite.
Apart from temperature there may be ojther factors in wild infected
sandflies which have not been reproduced in the experimental ones.
The following method was used to determine whether flagellates
can leave this .sandfly via the proboscis. Sandflies were infected on
cultures and were re-fed at various intervals. After eight days
they were allowed to feed through a membrane at room temperature.
on inactivated defibrinated blood which was subsequently examined
in fresh preparations and by culturing on Shortt's N.N.N. In six
experiments in which a total of seventeen sandflies with eight to
seventeen days* old infections fed through membranes, the result
was negative. In two experiments in which infected sandflies were
kept at 37° C. for half an hour before being placed in the feeding
apparatus, positive results were obtained.
Experiment I. Two sandflies fed 22. it. 27 on emulsion of
L, tropica (4,000 flagellates per cmm.), re-fed on puppy 27.11.27.
Re-fed on a solution of haemoglobin through membrane, 30.11.27.
After the feed a part of the fluid from the membrane was sown
on two tubes of Shortt*s N.N.N. , and the remainder examined in
fresh preparations.
Result : In fresh preparations three solitary flagellates were
found. The tubes of N.N.N. were subsequently found contaminated.
The two sandflies died 3. 12.28. Both were found heavily infected.
In one the upper part of the cardia was choked and no flagellates
were found in the stomach. In the other the cardia was choked and
the stomach was also heavily infected. In neither sandfly was the
proboscis found infected although the proboscis of one or both
sandflies was probably infected on 30.11.27.
Experiment 2. Seven sandflies fed 19.1.28 on an emulsion
of L. tropica, 3,000 flagellates per cmm. Sandflies kept at 37° C.
23.1.28 re-fed. 27.1.28. Three sandflies re-fed through a membrane
on inactivated rabbit blood. A part of the fluid from the membrane
was sown on a tube of Shortt*s N.N.N.-Agar. The remainder was
examined in fresh preparations. In nine preparations not a
single flagellate was found.
Result : 2.2.28, the tube of Shortt*s N.N.N. was examined and
found positive. The culture was continued and found infective for
sandflies no less than the parent strain (sixty sandflies fed and fifty-
seven became infected). The strain was passed through a mouse
and cultured and was still found to maintain its infectivity (147
sandflies fed and 129 became infected).
One of the sandflies died 30.1.28, and the stomach and cardia
were found heavily infected. The second sandfly died on 31.1.28,
and was fixed in Carnoy. Sections sihowed a heavy infection in
phar3mx, cardia and stomach. The third sandfly re-fed on 31.1.28,
15
was killed immediately after the feed, and was found heavily infected
in cardia and stomach.
The positive result obtained was quite unexpected as it was
thought that flagellates in the proboscis are incapable of dividing
until they enter a vertebrate host.
In neither of the positive experiments could flagellates from
the rectum have entered through the membrane, because in the
feeding apparatus the rectum points obliquely downwards during the
act of feeding. Even if flagellates would have been ejected on
the membrane, it is impossible to believe that they could have
penetrated into the fluid on the other side. The flagellates could,
therefore, have entered the fluid above the membrane only through
the proboscis.
In both positive experiments only very few flagellates passed
into the fluid during the act of feeding, in spite of the enormous
infection in the sandflies. It was thought that flagellates might
pass to the end of the proboscis and enter the duct of the hypo-
pharynx from where they would be bound to enter the wound
during the act of biting, but neither in dissected or sectioned
specimens were flagellates found in the duct of the hypopharynx.
We think there is a greater likelihood of obtaining a positive
result by the bite of a sandfly if the latter is kept at a temperature
higher than 22° C. Experiments are now in progress with sandflies
kept at 27° and 30° C.
In seeking for a possible insect vector of the Leishmanias of man,
we must bear in mind that these organisms do not live long together
with bacteria. Thus, insects with a rich intestinal flora, such as
the housefly, can be safely excluded as possible vectors. Mosquitos
often contain bacteria in their alimentary tract. Bed bugs can be
excluded as carriers because they do not occur in Baghdad.
Unfortunately, the intestinal flora of biting insects has not been
sufficiently studied. The alimentary tract of P. papatasii and
P. sergenti is bacteriologically sterile. Although the larvae constantly
devour bacteria, yet the adult never contains bacteria in its
alimentary tract. Sterilisation apparently occurs during pupation.
Bacteria which accidentally invade the alimentary tract of the
sandfly and multiply usually cause the death of the insect in a few
days. P. papatasii and P. sergenti are, therefore, favourable hosts
for JL, tropica.
i6
SUMMARY AND CONCLUSIONS
Two hundred and fifty-three sandflies, P. papatasiiy heavily
infected with L. tropica from cultures fed on twelve human beings
and a puppy.
There were more than five hundred bites, but the puppy and
eleven volunteers remained negative during an observation period
of one to fourteen months.
One case developed L. tropica on one of the areas on which infected
P. papatasii/e^f, but natural infection is not excluded as he lived in a
quarter where oriental sore occurred.
It has been shown by membrane experiments that L. tropica may
leave an infected P. papatasii via the proboscis.
L. tropica ex-flagellates in P. sergenti and undergoes a cycle of
development similar to that in P. papatasii and, after six days at
27° C., forms appear which are infective for man.
REFERENCES
Adlek, S., and Theodor, O. (1926). Further observations on the transmission of Cutaneous
Leishmaniasis to man from Pbhbotomus papatasii. Ann. Trap. Med. Parasitel.., 20 , 175-194.
[i^ 2 y). The transmission of Leisbmania tropica from artificially infected sandflies
to man. Ann. Trap, Med. ^ Parasitol.^ 21 , Sp-iio.
(* 9 ^ 7 )* behaviour of cultures of Leisbmania sp. in Pblehoiomus papatasii.
Ann. *Trop. Med. Sf Parasitol., 21 , 111-134.
(1928). The exit of L. tropica through the proboscis of P. papatasii. Nature, 121 ,
57 ^- 3 ^
(1928). The infection of P. sergenti with L. tropiia. Nature, 11 ^ 278.
Parrot, L., and Donatien, M. ^1927). Le parasite du bouton d^Orient chez le phlibotome.
Infection naturelle et infection experimentale. de P. papatasii (Scop.). Arch, de Vlnstitut
Pasteur d^Algerie, 6 , 9-21.
SiNTOM, J. A. (1925). The r6le of insects of the genus Phlebotomus as carriers of disease, with special
reference to India. Jnd. yi. Med. Res., 12 , 701-729.
Plate I
i8
EXPLANATION OF PLATE I
Sagittal section through the clypeus and mouth-parts of
Phlebotomus papatasii, showing mass of flagellates of L. tropica
between epipharynx and mandible (in the food canal).
Strain F. Infection fourteen days' old. Magnification 315 x.
B.C, — Buccal cavity.
E. = Epipharynx.
M. = Mandible.
H, ~ Hypopharynx.
L, ™ Labium.
F. = Flagellates of L. tropica.
ADDITIONAL EVIDENCE ON THE
OCCURRENCE OF L. TROPICA IN
WILD PHLEBOTOMUS PAP AT ASH
BY
S. ADLER, M.B., Ch.B.
AND
O. THEODOR, Ph.D.
{Microbiological Institute ^ Hebrew U niversity , Jerusalem)
{Received for publication 17 January, 1929)
The authors (1925 and 1926) recorded three experiments in
which Herpetomonas from naturally infected sandflies, Phlehotomus
papatasii, caught in Jericho, were inoculated into man and produced
oriental sores in two cases and a subcutaneous nodule containing
L.D. bodies in one case. The diagnosis of P. papatasii was
made because no males of other species which bite man were found
in Jericho and at the time the work was done no characters of specific
value for females of the genus Phlebotomus were known.
Subsequently (1926) the authors described the diagnostic value
of the pharynx in P. papatasii,
Sinton (1927) criticised the diagnosis of P. papatasii made by the
authors, and pointed out that a diagnosis based on negative and
not on positive evidence was not conclusive.
Knowles (1928) stated that, working in Calcutta, Smith failed
to infect laboratory bred P. papatasii by feeding them on oriental
sores rich in L.D. bodies. Knowles implied that the positive results
recorded by other authors were probably obtained with P. sergenti
wrongly diagnosed as P. papatasii.
This criticism is not applicable to the experiments recorded
by the authors (1927), in which L, tropica was transmitted to man
from artificially infected sandflies,, for in these experiments laboratory
bred sandflies were used and the pharynx was regularly examined.
(The diagnostic value of the pharynx was discovered towards the
end of 1925.)
19
zo
Strains of L, tropica vary greatly in their inf activity for
P, papatasii. While some strains produce a high infection rate
even when a small number of parasites are ingested, others produce a
slight infection rate even when very large numbers of parasites are
ingested. Smith's experiments prove that some strains of L. tropica
are completely non-infective for P. papatasii.
Although Larousse (1924) has recorded P. sergenti from Palestine,
we have never come across a single specimen of this species during
four and a half years’ collecting. In 1926, 1927 and 1928 we bred
about 4,000 sandflies from females caught in Jericho, over 8,000
from females caught in Jerusalem, and almost 1,000 from females
caught in Rosh Pinah (near Lake Tiberias), and we have never once
seen a single specimen of P. sergenti in this material. Nevertheless,
Sinton’s criticism is legitimate as far as the experiments with
Herpetomonas from wild sandflies caught in Jericho are concerned,
for there is a possibility, however slight, that P. sergenti, when
present in small numbers, may be overlooked. This possibility is
indeed very slight, for the male of P. sergenti is so characteristic that
it can be diagnosed readily with the naked eye even when it is sitting
on a wall. The female, however, can only be identified by the
character of the pharynx and spermathecae.
In the case of the wild sandflies used for inoculation experiments,
a part of the material was fixed on slides, stained and mounted. The
slides were recently re-examined and the head of only one sandfly
was found. This sandfly was caught in Jericho, 8.9.25, and was
dissected 9.9.25. Flagellates were found in the oesophagus,
oesophageal diverticulum, mid-gut and hind-gut. Part of the
flagellates was inoculated into a human being and produced a sub-
cutaneous nodule containing numerous L.D. bodies. Cultures were
obtained from the lesion and the strain has been maintained
continuously on Locke-Serum-Agar. Although the lesion was
atypical, there is no doubt that it was caused by L. tropica for direct
inoculation from this lesion into a human being produced a typical
oriental sore.
Examination of the mounted head showed a pharynx typical of
P. papatasii. The occurrence of Leishmania tropica infective for
man in wild P. papatasii is, therefore, proved concltisively.
21
REFERENCES
Adler, S., and Theodor, O. (1925). The experimental transmission of Cutaneous Leishmaniasis
to man from Phlebotomus papatasii. Ann. Troj[j. Med. & Parasitol.^ 19 , 365-371.
(1926). Further observations on the transmission of Cutaneous Leishmaniasis
to man from Phlebotomus papatasii. Ann. Prop. Med. & Parasitol.^ 20 , 175-194.
(1927). The transmission of Leishtnania tropica from artificially infected sandflies
to man. Ann. Trop. Med. & Parasitol.^ 21 , 89-110.
Knowles, R. (1928). An introduction to Medical Protozoology. Thacker, Spink & Co. Calcutta,
p. 191.
SiNTON, J. A. (1927). Notes on some Indian Species of the genus Phlebotomus. Part XVIII.
Indian Jl. Med. Res., 14 , 947-953.
TERNIDENS DEMINUTUS (Railliet & Henry)
AS A PARASITE OF MAN IN SOUTHERN
RHODESIA ; TOGETHER WITH OBSERVATIONS
AND EXPERIMENTAL INFECTION STUDIES
ON AN UNIDENTIFIED NEMATODE PARASITE
OF MAN FROM THIS REGION
BY
J. H. SANDGROUND, Sc.D.
(Department of Tropical Medicine, Harvard Medical School, Boston)
(Received for publication 24 January, 1929)
Plate II
In October, 1927, Dr. X., an American Medical Missionary, was
referred to the writer for an opinion on the intensity of a * hookworm '
infection which the patient harboured and which, it was considered,
might have been responsible for his ' run down ' condition.*
The patient had spent more than twenty-five years in medical
missionary work in Portuguese East Africa (Mozambique) and in
the eastern portion of Southern Rhodesia. Within the past few years
he had commenced the examination of the stools of many of his
patients for parasites and had been able to show that ' hookworm '
infection, previously unrecognised in this locality, was widespread
(ca. 82 per cent.). The attention of the Government public health
laboratory was drawn to this high incidence of infection, and some
worms secured by Dr. X. after anthelminthic treatment of a native
with carbon tetrachloride were submitted to the laboratory. The
situation has been reported upon briefly by the medical director
under the paragraph heading ‘ Hookworm ' in the ‘ Report of the
Public Health for the Year 1925, Southern Rhodesia ' (p. 19).
In September, 1926, our patient had made an examination of
his own stools, and had found a few nematode eggs which he con-
* llie writer is indebted to Dr. George C. Shattuck, for the opportunity of examining the
patient, and also to the patient for his hearty co-operation'in prosecuting these studies.
23
sidered similar to those found in the faeces of patients at the mission
station. These eggs he believed to be those of Necator americanus.
In our laboratory, stools were examined by the Willis-MoUoy
salt flotation method which furnished a small number {3 to 10 per
preparation) of Strongyle eggs. The eggs (see Plate II, fig. A and
photomicrograph, Text-fig. i) are thin-shelled, and somewhat
asymmetrical, being slightly less convex on one side than on the
other. One pole is Usually seen to be more pointed than the other.
Immediately after passage from the body, the eggs are in an
advanced state of segmentation, 16 or more cells having already
been formed. The eggs range in size from 72^« to 103/^ by 37/^ to 45^-.
The mean- measurement of 30 eggs taken over a period of months
was 84-5// by 41-3//.
Fig. I. Photomicrograph of egg found in fresh faeces, x 450.
In consideration of the fact that the eggs of the parasite under
investigation were (i) considerably larger than those of either
Ancylostoma duodenale or Necator americanus, (2) that they were
markedly different in shape, and (3) that they were deposited, in
a more advanced stage of cleavage, the writer was convinced that
the infection was distinct from the usual hookworm infections
of man.
Our first opinion was that the infection might be with a species
of Trichostrongylus, such as T. instahilis, T. vitrinus, etc., which
have on several occasions been encountered in man in Africa. The
possibility of an Oesophagostome infection was also to be considered.
To establish the identity of the parasite and to procure information
of its life-history, a systematic study of the infection was under-
taken. Infection experiments were planned, since our patient,
who was on furlough in the United States, expected to be ordered
abroad in a short time. In the meanwhile a letter had been written
to the mission station in Rhodesia requesting that samples of
preserved stools of infected natives be forwarded, together with
^5
the few worms that had previously been retrieved from a patient
there after treatment. The following notes summarise our observa-
tions on the biology and life-history of the parasite.
Development of the egg : — Entire stools were cultured in the
ordinary way after mixing thoroughly with a generous quantity of
animal charcoal. At room temperature the development of the
larva within the egg is completed in about thirty hours. On
emerging from the egg, the larva is of the typical rhabditiform
type (Plate II, fig. b ). It measures about 320/^ in length and is
i8/i broad near the middle of the body. The buccal cavity is
cylindrical and about 12-5// long, this being approximately equal to
the breadth of the body at the level of the base of the buccal cavity.
The oesophagus is 014 mm. long. The distance between the
anus and tip of the tail is 43//, and the tail tapers in a uniform
manner to an acute point. There appear to be no outstanding
morphological differences between this larva and the corresponding
larvae of the common human hookworm.
After a short period of feeding in the open, which is accompanied
by a certain amount of growth, the larva undergoes an ecdysis.
The early stage larva is indistinguishable from the first stage.
Growth proceeds and the passage from the second to the third, or
infective, stage is marked by a metamorphosis which chiefly affects
the structure of the buccal region and oesophagus of the larva,
transforming the latter from the rhabditiform type to the simple
claviform or filariform type. The infective or filariform larvae
develop in cultures incubated at 30X. in from 72 to 96 hours. They
range in size from 700// to 780/^ in length by 20^ to 21// in greatest
breadth. The morphology of this larva is illustrated in Plate II,
figs. D I and D2. It may be distinguished from the infective larva
of the hookworms in that it is at least from one-sixth to one-third
longer and its oesophagus is relatively smaller, being in this case
little more than one-tenth the total body length. Morphologically,
very distinct differences can be observed in the finer structure of
the anterior end, and in the structure of the slight swelling at the
posterior extremity -of the oesophagus. A very characteristic
peculiarity, which readily serves to distinguish this larva from the
corresponding larvae of the hookworms and related human parasites,
is the shape of the caudal extremity. In the hookworms the caudal
i6
region tapers gradually and uniformly to an acute point. In the
present form, the tail region tapers gradually, but terminates
abruptly in a truncated stump (Plate II, fig. D2).
Biology of the Infective larva : — ^The third stage larva, like the
corresponding hookworm larva, remains ensheathed in the cuticle
of the second stage larva. But, unlike the hookworm larva, this
sheath is retained, apparently, throughout the period of free life
and it furnishes the larva with a high degree of resistance against
desiccation. When water containing larvae has almost completely
evaporated (as in a watch-glass that is exposed) the larvae commence
to migrate up the side of the vessel in an endeavour to escape to
a moister ambient. On finding themselves in an environment free
from moisture, the larvae curl up in a characteristic watch-spring
coil. They may frequently be found in masses on the sides of
a watch-glass from which the water has evaporated. In an atmo-
sphere which is relatively humid, such coiled larvae remain alive
for a considerable length of time. Thus an old faecal culture
exposed to desiccation for more than seven weeks so as to become
quite dry yielded many larvae when placed in the Baermann isolating
funnel. Larvae which had been permitted to become completely
desiccated and to remain exposed on a slide for three days were,
when re-examined, seen to be in a much shrivelled condition with
the internal organs vacuolated. The larvae straightened out on the
addition of water, and in about an hour were moving in a perfectly
normal manner. This may be contrasted with the great sensitiveness
that the larvae of the hookworms exhibit to desiccation even for
a matter of a few minutes. The movement of the larva is con-
siderably more sluggish than the active swimming of the infective
larvae of the hookworms. They are practically unstimulated by the
application of moderate warmth and consequently their isolation
from ciUtures by the Baermann method is unsatisfactory. This
method of isolation was, however, used since it was more practical
with the lightly infected cultures that we were using than the
alternative method of trapping larvae that migrate from cultures
into surroimding water. Cultures placed in the isolating funnel
were still yielding larvae after two days.
The sluggish movement of the larva, together with its lack of
marked thermotropism suggests clearly that infection of the host
27
is by way of the mouth rather than by the penetration of the skin,
as normally occurs with the hookworms. Unfortunately, larvae
were secured in such small numbers that experiments to test their
ability to penetrate the skin were not warranted. An attempt at
the experimental infection of a rabbit was without result. Attempts
were made at the experimental infection of dogs and of a monkey,
but mature parasites were not found at our subsequent examination
of the alimentary tract of these animals.
A HUMAN INFECTION EXPERIMENT
Since the departure of the patient representing the source of our
material was imminent, and in order to avoid the loss of further
opportunity to study this unusual parasite, the voluntary infection
(to a light degree) of a human subject was decided upon prior to
attempting to dislodge the parasites in the original infection by
anthelminthic treatment for identification. On January 7, 1928,
twenty-seven young filariform larvae were placed in a hard gelatine
capsule and swallowed. Frequent examination of the stools by
concentration methods had been negative, when, on January 30th,
an additional fifty active larvae were swallowed in water. Six
examinations were made later, but eggs were found in the stools for
the first time on March 21st. These eggs were identical with those
from the original infection. The infection has persisted now for a
period of about nine months, without any apparent decrease.
The number of ova in the stools is very small, indicating that the
infection is a very light one. No untoward signs or symptoms are
evident.
At this point in our investigations, in response to our request,
we received a small sample of formalin preserved faeces of an infected
native from Southern Rhodesia, together with eight worms which
had been saved from stools washed after treatment. On examining
the faeces, several eggs were found similar in size and shape to
those which we had been studying.' All of the eight worms (of
which two were males) on examination proved to be Ternidens
deminutus (Railliet and Henry, 1905). In consideration of this we
felt justified in expressing some doubt as to the general ' hookworm '
infection in this region being due to either Ancylostoma or Necator.
28
ATTEMPTS TO SECURE THE PARASITE FOR ZDENTIFICATIOH
BY TREATMENT
Seeing that some degree of success had been secured in Rhodesia
in expelling the parasite with carbon tetrachloride, we decided to use
the same drug in the present case. Since this drug, as a rule, has
a very low toxicity, 4 c.c. instead of the usual 3 c.c. was administered
on an empty stomach after preliminary purgation with magnesium
sulphate. The drug was well-tolerated. Stools, immediately after
passage on the first day, were very carefully washed through a fine
screen without any worms being recovered. They were likewise
washed on the three days following with the same disappointing
result. A week later and on several subsequent occasions eggs
were found m the stools in apparently undiminished numbers.
The patient then left the country.
Some time later, an attempt to retrieve the parasites from our
experimentally infected case was made. After preliminary purging,
5 c.c. of tetrachlorethylene were taken in a hard gelatine capsule.
The stools were washed for three days through a fine isieve, but no
worms were recovered. The eggs still appear regularly in the faeces.
On the basis of evidence already available, it appears probable
that Ternidens deminutus, like species of Oesophagostomum,
Triodontophorus, etc., is a form which, at least in its early life,
inhabits cysts in the mucosa and wall of the large intestine (caecum
and colon). If this is later substantiated, since it is not unusual
to find that anthelminthics are effective only against parasites
which live exposed in the lumen of the small intestine, the negative
results. following the treatment in our cases may be accounted for.
THE PROBABLE IDENTITY OF THE PARASITE
The failure of our anthelminthic to dislodge the parasites in the
infection has prevented the possibility of making a specific
determination. Until an opportunity is obtained to follow an
infection to necropsy and in this way to secure the adults, or to
obtain a richer source of material, for infection experiments in
apes, we can do no more than suggest-tbe probable ide^ttity of the
parasites. •
Although the eggs are definitely those of a Strongyle nematode.
29
there is ample evidence to prove that it is neither Ancylostoma or
Necator. The size of the eggs is such that Trichostrongylids cannot
be eliminated from consideration, but there appears to be no further
evidence to incriminate a species of this group of parasites. The
possibility of the infection being due to a species of
Oesophagostomum, such as have on occasion been found to parasitise
man, may be ruled out, since the eggs of these species are slightly
smaller and are not asymmetric in shape. Further, the tail in the
rhabditiform larva and in the infective larvae of Oe. apiostomum
(— Oe. brumpti in the opinion of Leiper) is figured and described by
Walker (1913) as being very elongate and filiform. This
characteristically attenuated tail is also observed in the larva of
Oe. dentatum of the pig, according to Goodey (1924) and
Oe. columhianum of sheep, according to Veglia (1924). This is in
contrast with the larvae secured from the present infection.
The material of Ternidens deminutus received from Rhodesia is,
unfortunately, such that even when a female specimen was teased
apart, eggs were not obtained, so that the direct comparison of the
eggs cannot be made. However, Leiper (1908) gave the measure-
ments, 6oyM to 80^ by 40^, as the size of the eggs in the uterus of
preserved female Ternidens deminutus. The larger range in Leiper’s
measurements agrees very well with the mean size of the eggs in the
infection we have studied. The shape of the eggs, although not well
depicted by Leiper, also seems to be in agreement. Evidence to
supplement the idea that the infection which we have been
investigating is Ternidens deminutus is to be found when we review
the previous records of infection with this parasite and its geographic
distribution in man.
Railliet and Henry (1905), while examining the collection of
parasitic nematodes in the Museum of Natural History in Paris,
found a vial containing parasites collected in 1865 at autopsy of a
native of Mayotte, in the Comoro Islands, off the coast of Portuguese
East Africa. The patient had succumbed to an anaemia, and in the
intestine, the walls of which were considerably thickened and
presented numerous petechial haemorrhages of the mucosa, nematodes
were found. The medical officer who had performed the autopsy
identified these as Ancylostoma duodenale and considered them the
cause of the clinical condition. In this vial, Railliet and Henry
found two nematodes, a male and female, which were new to science
and for which the name Triodontophorus deminutus was proposed.
Later the same authors, on revising the classification of the
Strongylidae, withdrew the parasite from the genus Triodontophorus
and erected the new genus Ternidens for. its reception, placing the
genus in the sub-family Oesophagostominae. Up to the present
this genus is represented by a single species.
The second record of T. deminutus is by Leiper (1908), to whom
Turner, a medical officer on the mines of the Witwatersrand (Transvaal)
sent some hookworms recovered at autopsy from the intestines of
two natives of Nyassaland. Turner noticed that among the worms
there were a few females, slightly larger than the others, occup5dng
what he thought to be an abnormal habitat, the large intestine, the
mucosa of which showed congested patches. These worms were
identified by Leiper as Ternidens deminutus. Leiper also found a
single specimen, probably of the same species, in a gorilla from the
London Zoological Garden. Brumpt has found specimens in Macacus
sinicus, and the species has also been reported from Macacus
cynomolgus in Saigon.
Smith, Fox and White (1908), in America, reported the finding of
Globocephalus macaci (= probably T. deminutus) together with a
species of Oesophagostomum in the intestine of Macacus nemestrimus.
One of the two species of parasites occupied submucous cysts, but
the authors were unable to state which of the two species was
encysted.
Summarising the limited information at present available, it
appears that Ternidens deminutus is primarily a parasite of Primates
(Catarrhinae) which probably serve as the reservoir hosts for man.
All human infections thus far recorded have been found in negroes
from Central East Africa. On the basis of the parasites received
by us from Southern Rhodesia, an additional case may be added to
the lists.. It seems probable from the evidence available that in this
locality, the infection is not an uncommon one. There has been a
history of confusion of this parasite with Ancylostoma duodenale and
Necator americanus. No case of infection has hitherto been diagnosed
in the living host, nor has the parasite been specifically identified
at the time of autopsy so as to permit a study of the habits of the
parasites and of the pathological changes that they may induce.
Further studies to provide information on these points are indicated.
3 *
REFERENCES
Goosey, T. (1924). The anatomy of Oesopbagostomum dentatum (Rud.), a nematode parasite of
the pig, with observations on the structure and biology of the free-living larva. Jl.
Helminthology^ 2 , 1-14.
Leiper, R. T. (1908). The occurrence of a rare sclerostome cf man in Nyassaland. Jl. Trop.
Med. & Hyg.,n, 181-184.
(1911)* Notes on recent and some new records of helminths in man, of which there are
few records. Jl. Land. &ch. Trap. Med.^ 1 , 16-19.
Railliet, a., and Hemry, A. (1905). Le Triodontopborus detninutus, nouveau Sclerostome de Thomme,
et la cachexia Africaine. Bull, du Mus. d'Hist. Nat.y Paris, No. 5 , 269-272.
Smith, A. J., Fox, H., and White, C. Y. (1908). Contributions to systematic helminthology.
Univ. of Penn. Med. Bull.^ 20 ) 283-294.
Veglia, F. (1924). Preliminary notes on the life-history of Oesophappstomum columhianum.
Ninth and Tenth Reports of Director of Vet. Educ. and Res., Union of South Africa, Pretoria,
pp. 811-823.
3 ^
EXPLANATION OF PLATE II
(All figures were drawn with the aid of the camera lucida. Magnifica-
tions are indicated by accompanying scales.)
A . Ova found in fresh stools.
B. First stage (Rhabditiform) larva.
C. Second stage (Rhabditiform) larva in process of transition*.
Di. Anterior end of third stage (Filariform) larva.
/)2. Posterior end of third stage (Filariform) larva ensheathed in
cuticle of second stage larva.
NOTE ON THE OCCURRENCE OF
CRITHIDIA IN PHLEBOTOMUS
MINUTUS VAR. AFRICANUS- IN
NORTHERN NIGERIA
BY
A. W. TAYLOR
OF THE TSETSE INVESTIGATION, NORTHERN NIGERIA
{Received for publication 20 February, 1929)
Few instances have been recorded of crithidial infections in
Phlebotomns species. Wenyon (1926) states that flagellates found
by Mackie in P. minutus in Assam were crithidia, and suggests
that the flagellate concerned may represent a trypanosome of a
lizard on which these sandflies are known to feed.
Wenyon (1926) also suggests that flagellates found in P. papatasii,
in Italy, by Laveran and Franchini (1920), and named by them
Herpetomonas phlebotomus, may be crithidia.
The observations recorded below were made on Phlebotomus
minutus var. africanus, the only species common at Sherifuri. This
sandfly is most numerous during the dry season months of April and
May, when it attacks man.
It was observed in the course of the wet season of 1928 that
P. minutus var. africanus, although rarely seen elsewhere, was
present in large numbers in a cage containing monitor lizards
(F. exanthematicus and F. niloticus). The sandflies could be seen
daily feeding on these lizards and also on a small python in an
adjoining cage. Although these cages were on the verandah of the
laboratory, sandflies were never seen in the building, and apparently
were feeding entirely on reptiles.
Examination of the blood content of the mid-gut in 155 of these
sandflies containing recognisable blood, showed that over 99 per cent,
of the blood was reptilian. A reptilian haemogregarine was common
in many of the guts examined.
During August and September, 1928, 304 Phlebotomus (301 $ 9,
3 <?c?) Vere caught in the lizard cage and dissected. In 31
33
34
flagellates were found in the mid-gut, giving ati infection rate of
10*2 per cent. In all the infected sandflies examined, thf infections
were con^ned to the mid- and hind-gut. ^
Stained smears of the infected guts proved the infections to
consist entirely of T.-~grayi type crithidia/ their moiphology corres-
ponding with the description of T. grayi crithidia given by Minchin
(1908).
Light infections consisted only of the short, broad type of crithidia,.
while heavier infections contained also long slender forms. In no
case were trypanosomal or spherical forms seen.
The^ heaviest infections were found in sandflies in which digestion
was far advanced (two to three days after feeding). Sandflies
containing fresh blood, and those in which digestion was complete,
were negative. Between 1923 and 1928, the bloods of 106 Varanus
of both species have been examined at Sherifuri, and 77, or 68-6 per
cent, have been found to be infected with T, varani. Lloyd, Johnson,
Young and Morrison (1924) showed that G. tachinoides fed on infected
F. exanthemodicus developed a flagellate infection of the mid-gut,
which was indistinguishable from crithidia of T. grayi.
Six of the Varanus, which were in the cage fr6m which sandflies
were obtained for dissection, were subsequently^ killed, and in four
of them the blood was found to contain tr3rpanosomes. The python.
35
which was a possible alternative source of infection, was killed, and
its blood proved on examination to be negative.
The flagellates in P, minutus var. africanus described above were
evidently crithidial forms of T. varani undergoing incomplete develop-
ment in the sandfly ; it is possible that their occurrence is accidental.
REFERENCES
Lloyd, Ll., Johnson, W. B., Young, W. A., and Morrison, H. (1924). Second report of the
tsetse-fly investigation in the Northern Provinces of Nigeria. Bull, Ent, Res.^ 15 , i.
Minchin, E. a. (1908). Investigations on the development of trypanosomes in the tsetse-flies and
other diptera. Quart. Jl. Microscop. Sci.^ 52 , 159.
Wenyon, C. M. (1926). Protozoology. London.
THE RELATIONSHIP BETWEEN ECONOMIC
DEVELOPMENT AND RHODESIAN SLEEPING
SICKNESS IN TANGANYIKA TERRITORY
BY
GEORGE MACLEAN, M.B., D.T.M.
SLEEPING SICKNESS OFFICER, TANGANYIKA l-ERRITORV
{Received for publication 25 February, 1929)
With Map
Before the War there was very little Rhodesian Sleeping Sickness
known in what is now Tanganyika Territory, and what was known
was confined to the Southern part of the country. Since the War
three large outbreaks have come to light, one in Mwanza, South-east
of Lake Victoria, one in Ufipa and Tabora, and one in Liwali. The
last appears to have been a local epidemic superimposed on endemic
conditions (Dye, 1927) while, in the case of the other two, years of
enquiry have failed to elicit any information about previous endemic
foci.
It may not be possible at this stage to clear up definitely the
atmosphere of conflicting theories that surrounds the genesis of
these outbreaks, but it may be of some interest to endeavour to
trace some of the changes that have taken place in tsetse distribution
in comparatively recent years. (To appreciate the effects of the
changes to be described it is necessary to bear in mind that the
t5rpe of open country such as is met with in Central Mwanza, all the
Districts of Tabora, and numerous other places would revert to
tsetse forest if that forest were not kept at bay by human activity.
Abandon cultivation at the forest edge and, unless possibly very
intense grazing prevents it, the forest will rapidly spread over the
abandoned ground, and generally, tsetse infestation will follow.)
In an enquiry such as this one naturally turns first to records of
early travellers^ but- these, records, unfortunately,^ are lacking in
the type of information required. For instance, Stanley, on his
way to find Livingstone, passed through a large open forest which
e1d:ends, with few breaks, for tens of thousands of square miles and
37
38
(now at least) largely infested by Glossina morsitans, between Tabora
and Ujiji. Both these travellers returned through the sanie forest,
and again Livingstone when he set out on his last journey passed, in a
different direction, through the same forest ; but though we meet
BZHARAICULO
district
Southern
Usaabiro
TABOHA
DISTRICT
Nyonga
CR ' —
DlAOitAM TO ILLUSTRATE REVERSION FROM OPEN COUNTRY TO TsETSE BuSH
IN DIFFERENT DISTRICTS.
=-= ■: s= Country once open reverted to bush by 1925.
|{ tf } 4 ' -' =*= Country still open.
Scale (rough estimate only) : i inch = 4 miles.
UFIPA
DISTRICT
Ilunde
with a reference or two in the latter’s journal which places tsetse
within perhaps 50 miles of Tabora town on the South, there is
nothing to indicate that this was its boundaty, or what, in the
infested part, was the everyday contact between man and fly. , >
39
V I C T 0 R I AjjanllllljfipollwiJfs'X;^^
'’•'‘’t!-' 'i Jr CjuspwM
/ 1'
1 (iwrXMM IJII
/ mm MoSHiiK-
A rX.S H a L
I^SO V J^N I Bilii »D«r|-»^Uraj|
rindl .1 '
Ik.*:.'
Map of Tanganyika Territory,
Rhodesia = , Provinces = T A B 0 R A.
Tsetse Distribution (small clearings in the Districts = TABORA.
general forest not shown) = |j|||||||||||||||||| Towns = • Tabora.
Provincial Boundaries = Chiefdoms = Urambo.
Scale : i = 5,000,000
After the Veteriiifry Dept. Tsetse Map, slightly modified.
40
Stanley's record of his journey from Uganda to Ujiji, in 1876, is of
interest in that, though he does not mention tsetse, he gives the
population of several towns, among them the capitals of Usambiro
and Ushirombo (Sorombo), with 2,000 and 5,000 people respectively.
(Only a few people remain in these now and both are surrounded
by young tsetse infested forest, while the second of them is now in the
midst of Sleeping Sickness area.)
What information is lacking in such records, however, is to a
limited extent supplied by natives, and this information can
frequently be confirmed by observing the state of the trees and land
in different parts of the forest.
Information of more than two generations back is generally very
vague. It would appear that some tribes, like the Wakamba (in
Mwanza and Kahama), reclaimed forest lands when they wished to
extend ; while others, like the Masai (in Arusha), set out to conquer
and seiz^ territory already occupied ; but whatever the conditions
may have been in the distant past, it is certain that about two
geneiutions ago, in places like Ufipa, Tabora, and Kahama, tribal
wars compelled the people to live, for safety, in large communities
of a hundred families or more — sometimes as many as a thousand.
Round these settlements were the grazing and arable lands. The
main occupation of the people in the intervals of peace were
agriculture stock-raising. Whether there were then, as now,
professional fishermen who spent a large part of the dry season at
rivers infested with G. morsitans and G, swynnertoni, is not clear,
but it seems unlikely that the unsettled state of the country would
allow it to be as extensive as it is now. The bee industry which
now flourishes appears to have existed then only for local and
limited needs. Most communities had professional hunters. The
older people who remember those days are emphatic that isolated
family villages did not and could not exist then. Even when a
raid took place and was successful it rarely if ever resulted in the
building of small remote villages.
The usual result was that the sacked settlement was wiped out,
the survivors being taken as slaves or escaping to take refuge with
some friendly neighbour.
We thus find that in the days before European domination the
forest peoples lived in clearings where houses, wclk and a large
4 *
section of the arable land must have been almost or completely
tsetse free all the year round. While there were hunters and, possibly
also, honey-collectors and fishermen, the normal life must have
been such as reduced the contact between man and fly — even
assuming that tsetse was as numerous in the surrounding forests as
it is now — to a minimum.
From time to time during seasons of tranquillity a ' daughter '
community was formed. An area of virgin or semi-virgin forest was
chosen, the trees felled and a new settlement started. This was no
individual effort but an organised affair under the leadership of
some scion of the chief’s family. The new settlement was thus a
large one from the beginning.
With the coming of European administration this state of affairs
underwent a gradual change. Punitive expeditions played their
part in the early days in upsetting the old regime, but this was
only temporary and its effects were comparable to the results of the
old tribal wars. What was much more far-reaching and permanent
in its effects was the establishment of peaceful administration.
One of the earliest results was seen in the chiefdoms possessing
large numbers of slaves (e.g., Urambo, Usumbwa, etc.). Such of
these as had recently been taken from their homes and now liberated
by the German Government, grasped their opportunity and returned
to their own country. This was a serious matter for such chiefdoms
as depended on their slaves to till the land.
The next important result was the evolution of a new type of
forest village. 'With the suppression of tribal wars the necessity
for living in large villages for protection no longer existed. There
was now an opportunity for benefiting by law and order without
having to shoulder the responsibilities of citizenship and many natives
took it. It was now possible for a man and his family to go into
the forest and start a remote settlement on their own. The virgin
soil 5delded ample crops and they were comparatively free from the
control both of their chief and of the new administration.
The rise of this type of family village in the midst of tsetse has
been one of the most important predisposing causes in the
epidemiology of Rhodesian Sleeping Sickness.
This disintegration of the large communities, which commenced
more than a generation ago, is still going on. Its progress would
probably have been more rapid but for the fact that cattle labour,
are less ready to take part in it than others. When they do so they
usually leave their stock behind so long as it is healthy for them
to remain.
The next aspect of the situation was the demand for labour.
The country had to be developed as well as administered and on the
heels of the administrator came the trader and the planter. Houses
had to be built and roads and railways had to be made. Labour was
also required for the sisal and other plantations that were now
growing up.
In certain areas only a fraction of the labourers recruited for
these purposes returned to their old homes. They settled elsewhere^
sometimes taking their own womenfolk with them. This drain
on the population contributed still further towards the breaking up
of the large forest communities.
Finally the late War gave revolutionary force to the disintegrating
changes that were taking place. The oxigencies of the times made
it necessary to commandeer porters^ cattle, sheep, goats, etc., and
many communities date their tsetse problem from the time that the
army of one or other of the combatants passed through. Influenza^
followed with dire results.
With peace came a certain amount of reconstruction^ but two
important factors remained. Families still continued to live m
small bush villages, enjoying their hunting and general freedom from
control, the number of villages increasing as old lands became over-
cultivated or unpopular. •
People with a more modem bent left their forest homes
permanently to settle in the more populous parts of the country
and under more civilised conditions.
The demand for labour, at first small, rapidly increased. The
forest native, living, as he often does, far from markets and means
of transport, has found that labouring on an estate or on railways,
docks, etc., is a convenient means of getting his tax, and supplying
his general wants while, at the same time, he enjoys the advantages
of travel. ^ ^ ^
The labour of these people, who do actual work for only a portion
of the time that they are absent from their homes, is largely
lost to their chiefdoms ; local development is hampered, more land
reverts to bush and a vicious circle is established.
43
The protection afforded by cleared and cultivated or grazed land
is lost and at certain times of the year tsetse is found almost every-
where, occasionally even inside the houses. This applies to both
G. morsitans and G, swynnertoni. When this stage is reached all that
is necessary is the introduction of Trypanosome infection to break,
up what homes remain and complete the devastation.
There are some infected places where the situation is not so
acute, where for instance people, mainly fishermen, honey collectors,
or hunters, whose homes may be in open country, contract infection
while following their vocations ; but these are in the minority and
cause concern only in so far as they are threatened by the increasing
fly-infestation already described.
This, briefly, is the situation as it affects the chief Sleeping
Sickness districts, at least so far as Ufipa, Tabora, Kahama, and to a
lesser extent, Mwanza are concerned. But there is another and a
more hopeful aspect. Just as old forest settlements are dwindling,
modem enterprise is reclaiming vast stretches of bush, far plantationsy
in other parts of the territory, particularly near the coast, and it is
largely the people whose lands are being invaded by tsetse that have
done the actual work of reclamation for the plantations. -v
There are at present no accurate data available by which we
can calculate our gains and losses, but it is not improbable that at
least as much has been gained as lost. One important factor in
the situation is the great leakage of man power that is taking place.
The permanent homes of the labourers are frequently hundreds,
of miles from the scenes of work and many months are lost yearly in
travelling and loitering. It is possible that in course of time most
of the labourers, instead of maintaining their old homes, will tak;^
their families with them to live permanently on or in the vicinity
of the plantations on which they work. A movement of this nature
has already commenced on a small scale, but for various reasons —
such as attachment to their own chiefdom, tfie freedom of , forest
life, etc. — the movement is not popul^ir and is unlikely to furnish an
early solution of the problem. This drift of native activity towards
the plantations and the newer industries must continue for many
years and while it continues there will be a corresponding change,,
and a change for the worse unless dealt with, in the tsetse and
Sleeping Sickness situation. .
The picture which I have endeavoured to draw only depicts that
44
section of the population which, caught in the tide of modern enter-
prise, had no local interests strong enough to root them to their old
homes.
There is another section, living for, the most part in fly-free
or almost fly-free country, who are fast developing their local farming
resources. Unless this section specialises in stock raising to the
neglect of agriculture and thereby allow tsetse to encroach on them,
they stand to gain considerably and not to lose by modem progress.
It is the evolution of this type of community and what it stands
for in the way of native endeavour that must be aimed at in any
campaign against Rhodesian Sleeping Sickness. Successful agri-
culture is one of the most powerful weapons that can be at present
employed against any tsetse of the Morsitans group.
In taking stock of our prospects for the future the Sleeping
Sickness areas of the territory may be regarded as divided into
three ill-defined zones. In the first zone the people can be settled in
large communities under conditions similar to those enjoyed by that
section of the population just described, by selecting and clearing
unoccupied land for them on the borders of the open country. In
these new settlements large numbers of the young men may leave
their homes and go out to work and see the world, but most of them
will come back. What leakage may occur is likely to be made good
by natural increase and by immigration from less favourable localities.
The measures necessary to ensure successful agriculture in these
communities need not be entered into here.
In the other two zones, where, for various reasons, people must
still have their homes in the forest, the dangerous family village
already described can be eliminated by settling the people in large
clearings. It has already been shown in Tanganyika Territory that
this can be safely done even in the middle of an epidemic.
In the second of these zones transport difficulties are compen-
sated for by some local advantage such as rich soil, a good honey
forest, etc. As in the first zone the people are likely to maintain
numerical strength in spite of a certain leakage; •
In the third zone the people, situated far from the main markets
and having no special local advantages, can only hold their own by
accepting a lower standard of livingr”4ienerally speaking these
settlements are likely to dwindle gradually as the people drift
45
towards the more favoured parts of the country and, probably, the
best that can be done for them is to show them how to keep their
homes as free from tsetse as possible and at the same time develop
such resources as they possess. In a country whose possibilities
both in mineral and farm products are still so imperfectly explored
it would probably be a mistake to eliminate by wholesale evacuation
even these outlandish settlements, at least, so long as they do not
remain a serious reservoir of trypanosome infection.
SUMMARY
Before the days of European domination the people of Tanganyika
Territory lived for the most part under conditions which made it
difficult for Rhodesian Sleeping Sickness to get a firm footing.
The freedom that followed the coming of the European resulted
in the evolution of a type of bush family village which became a
danger to health because of the close contact between man and
tsetse that it made possible.
Some of the old large settlements shrank to the dimensions of
these villages from various causes, the chief of which were the
disturbances produced by the Great War and the re-distribution of
population that has resulted from the 6p>ening up of the country.
The situation can be met by encouraging native agriculture
where this can profitably be done. In places so remote that successful
development is problematical the people can be collected in settle-
ments large enough to be safe from extinction by Trypanosomiasis.
The people in these settlements have a tendency to drift towards
places where better conditions prevail. When this takes place on a
large scale the dwindling settlements will have to amalgamate for
self-protection, a process of gradual and orderly evacuation will have
set in, and continue unless some local attractive source of wealth
is discovered to turn the tide.
Once the bush village is compulsorily eliminated it should be
possible for reclamation and evacuation to go on in an orderly
fashion, as the exigencies of the general situation demand. It
should also be possible for native and non-native enterprise to go
on with no more antagonism than a legitimate rivalry for labour and
for markets.
ACKNOWLEDGMENTS
- 1 am indebted to Dr. J. O, Shircore, C.M.G., Director of Medical
and Sanitary Services, for advice and for permission to publish this
paper^ and to Major F. J. MacCall, M.C., Director of Veterinary
Services, for. permission to make use of his tsetse map of the Territory.
REFERENCES
Dyi, W. H. (1927). The relative importance of man and game n human Trypanosomiasis. Trans.
Roy. Soc. Trof. Med. & 1 87-198.
Shircore, J. O. (i9i3)> Parliamentary Blue Book, Minutes of Evidence, p. 136.
SWynnerton, C. F, M. (1923). The entomological aspects of an outbreak of Sleeping Sickness, near
Mwanza, Tanganyika Territory. Bull. Ent. Res.^ 13 , 317-320.
NOTES ON THE ANATOMY OF STILESIA
HEPATICA, AND ON THE GENERA OF
THE SUB-FAMILY THYSANOSOMINAE
: (INCLUDING AVITELLININAE)
BY
. T. SOUTHWELL
(Received for publication 26 February, 1929)
I. ON THE ANATOMY OF STILESIA HEPATICA
Amongst the Cestodes in the collection of the Liverpool School of
Tropical Medicine there are a large number of specimens from different
sources referable to the sub-family Avitellininae ; apparently the
collection contains all the known, together with a number of new,
species.
During the examination of this material the writer found one
species which at first seemed to present remarkable characteristics
in that there appeared to be four paruterine organs in each segment,
viz., two on each side, except in the very gravid posterior ones, in
which only two paruterine organs occurred, viz., one on each side. A
careful examination of the worm left no doubt whatever that the
species is Stilesia hepatica Wolffliiigel, 1903, and the opportunity is
here taken of supplementing the excellent accounts of the anatomy
of this species given by Stiles and Hassall (1893), and Gough (1911)
The worms were obtained from (i) Liver of sheep, Durban, South
Africa ; (2) Cobus cob, gall bladder and bile ducts, East Shore,
Lake Albert, Tonya-, Mr. Thwaite ; (3) Hepatic duct of goat,
Rhodesia, Professor Yorke ; and (4) Sheep, South Africa, A. W.
Noel Fillers, Esq., F.R.C.V.S.
They attain a length of about 50 cm. and a maximum breadth of
about 3 mm. A large number of the* anterior segments, i.e., those
containing the male genital organs, are extremely shallow and
resemble a pile of saucers. They have a length of about 20 ju and
a breadth of about 2 mm. ; those posterior segments which contain
the fully-developed paruterine organs have a length of about 320//
and a breadth of 1*2 mm. The posterior margin of one segment
47
48
overlaps the succeeding segment, as shown in figs. 5, 6, and g, thus
enabling one to determine, without any uncertainty, the important
point as to which margin is anterior and which is posterior. The
genital pores are irregularly alternate and are situated near the
middle of the lateral margin of the segment. The pore leads into
a rather long and narrow genital atrium, at the base of which the
male and female genital ducts open. The cirrus sac is invariably
anterior and ventral to the vulva on both sides of the strobilus (fig. i).
The longitudinal muscles, according to Gough,
* are in two layers, an inner consisting of bundles of about 12, the outer of 3 or 4
muscles, the transverse muscle is weak as is also the dorso-ventral muscle.'
Figure 2 is a camera lucida drawing of a transverse section of the
male mature .part of the worm. It will be seen that the longitudinal
muscles are in one layer only. The bundles are all very very small,
each consisting of from about two to twelve fibres ; no trace of a
sub-cuticula layer of longitudinal fibres could be found in transverse
sections from different parts of the strobilus. In our specimens the
circular muscular layer is well developed.
' The male genital organs have been fully and accurately described
by him, and need not be further considered.
He remarks that,
‘ There is but one ovarium, lying on the pore side, between the dorsal and ventral
canals, nearer to the ventral than to the dorsal canal.’
He figures it as situated amongst the testes. An examination
of a large quantity of material, including whole mounts, transverse,
longitudinal and horizontal sections, leaves no doubt that Gough's
statement is correct. In transverse sections it is seen situated
ventrally, between the ventral and dorsal excretory vessels (fig. 2).
Directly dorsal to it is the lateral poral dilatation of the transverse
uterus, whilst on the aporal side a similar dilatation develops.
From the base of the genital atrium the vagina first dilate into a
vulva which lies dorsal to the cirrus sac. Near the median extremity
of the latter organ the vagina narrows and pursues a slightly sinuous
course almost to the level of the dorsal excretory vessel, where it
bifurcates, one branch going to the more ventrally mtuated ovary
(which quickly atrophies), and the other branch to the lateral poral
dilated termination of the uterus, which, as noted above, is situated
immediately dorsal to the ovary (fig, 2}. Although both Stiles
49
and HassaD, and Gough state that a receptaculum seminis is present*
in our specimens the vagina nowhere dilates, i.e., a definite
receptaculum seminis is absent. Gough points out that,
‘ The uterus is double, one uterus lying close to the ovarium, the other on the other
side of the proglottid in the corresponding position. The two uteri are connected
by a duct, the inter-uterine duct, which, however, may be morphologically but
the median portion of the uterus.’
Fig. 2
The uterus is, therefore, in reality single, roughly dumb-bell shaped,
extending across the segment, with one lateral dilated extremity
dorsal and dose to the ovary, and the other lateral dilated extremity
so.
on the opposite side of the segment, the two being for a short time
connected by a narrow tube which runs across the segment. Stiles
refers to eggs which
‘ travel across the segment and enter the uterus on the other side .... at first
no ova are seen in either uterus, then they appear in the uterus on the pore side,
and at the same time a broken line of ova can be seen extending across the segment
toward the opposite uterus ; the latter is next observed containing ova, while no
ova can be distinguished in the median field. I am forced to admit that in no one
segment has it been possible to find a continuous line of ova extending across the
entire median field, but by combining several segments a diagrammatic line of ova
may be constructed which extends from ovarium [/tV T.S.] to uterus. An interesting
point in connection with this wandering of the ova across the segment is that the
young ova, especially those found in the median field, have no definite form, a fact
which points to their being capable of amoebic motion.’
Gough, in his figures of S. hepatica and S. glohipunctata, shows the
duct, and in his account states that it exists, but he does not describe
it.
The duct was very clearly seen in our sections (figs. 3 and 4) but
it should be noted that it is an extremely delicate and transient
structure, having a diameter of about 16^, only found in a limited
number of segments, about twenty, which" are in a paxticulac stage of
development, viz., in those in which the lateral uterine dilatations are
SI
developed, and before the appearance of the paruterine organ. Ip
segments at this stage the tube is well defined and full of eggs,
which latter pass across in single file. The duct, however, quickly
atrophies, as shown in fig. 4, and the lateral globular dilatations of the
uterine tube, one on each side, do not, at any future stage in their
development, communicate with each other.
The paruterine organ begins to develop within the dilated lateral
extremity of the uterus on each side, almost as soon as the
uterine cavity appears. In the meantime there appears anteriorly,
and somewhat median to it, an almost solid, globular organ,
consisting of fibrous tissue arranged in concentric layers
which I shall refer to as the paruterine pouch (figs. 5, 6 and 7).
The two organs, on one side are in communication with each
other by a narrow aperture, as shown in fig. 8. The concentric
lamellar fibres from the paruterine pouch invade the cavity of the
paruterine organ and eventually become arranged in the form of
elongated columns ; it is into these columns that the eggs pass.
During this development the paruterine organ gradually becomes
less and less conspicuous, whilst the paruterine pouch becomes
increasingly prominent and large ; so that in whole mounts, and in
sections, there are to be seen two globular organs on each side of each
segment, situated between the dorsal and the ventral excretory
vessels. When the paruterine pouch is fully developed the lateral
dilatations of the uterus (i.e., the paruterine organs) have partly
atrophied and are indistinct, the result being that in each segment
there appears to be only one globular organ (paruterine pouch) on
each side of the segment. In some segments, the lateral dilatation
of the uterus (paruterine organ) on one side of the segment, partly
atrophies before the lateral dilatation of the uterus (paruterine organ)
on the other side of the segment. Consequently, in these segments,
under low magnifications, three globular organs only are to be seen,
two on one side and one on the other ; so that in segments situated
a little distance from the posterior^ extremity, there are in each
segment, two globular organs, on each side (one being the lateral
dilatation of the uterus containing the paruterine organ, the other
being the paruterine pouch) and they are approximately of the same
size. In the most posterior gravid segments only one globular organ
on each side of the segment is seen, viz., the paruterine pouch.
52
Segments between these two extremes show that the lateral dilatation
of the uterus containing the paruterine organ gradually gets less and
less and apparently finally disappears.
Stiles and HassaU, Gough, and Baer figure in the fixUy gravid
segments a very wide and prominent area full of granules, occupying
silmost all the middle of the segment, gradually taperiilg laterally on
each side to a bluntly-pointed cap-Bke termination which rests on the
53
anterior part of the paruterine pouch. A structure similar to what
these authors figure is often extremely conspicuous in the posterior
part of the strobilus, but it is not present in all strobila, whilst in
other strobila it is present in some gravid segments and absent in
others. On account of its position and appearance, especially in
whole mounts, it might easily be mistaken for a uterus full of eggs.
Having regard to the fact that, as we have seen above, the narrow,
median uterine tube which runs between the dilated uterine termina-
tions on each side quickly atrophies, the writer was unable to under-
stand the nature of the structure figured by the above authors, and
indicated also in my fig. 9. Careful investigation, however, revealed
the following facts : —
1. The granulations only occur in partly or wholly gravid
segments, and they are not quite, but almost exclusively limited
in distribution to the medullary parenchyma.
2. Even in the most gravid segments the granulations vary in
size from about 3/i to 25/t ; they show no cellular structure and have
a somewhat irregular outline.
3. They are not contained in a sac but lie free in the parenchyma
and are not in communication on either side with the uterus or
paruterine organ.
4. As noted above they are frequently entirely absent in some
54
gravid strobila ; in other strobila they are present in some segments
and absent in others.
Stiles states that,
‘ In many segments one sees at the posterior edge, especially in the lateral fields,
a row of small (4 to 8 /^) round or oval bodies which stain very dark in haematoxylin
or carmine. These same bodies are occasionally met with in the median field, but
their presence is extremely irregular. In general appearance they resemble, to a
certain extent, the calcareous bodies found in T. crassicollis, 7. solium, etc.’
The writer is of opinion that these granulations are probably
calcareous corpuscles which develop extensively in the increasingly
gravid segments.
The eggs produced by each segment of this and, in fact, by all
species of this genus, are few, usually about thirty, and are limited
in position to the uterus and paruterine organ on each side.
Fig. 9
II. ON THE GENERA OF THE SUB-FAMILY THYSANOSOMINAE
(INCLUDING AVITELLININAE)
In 1874, Rivolta described two worms from sheep in Italy, viz.,
Taenia globipunctata and T, centripunctata.
Railliet, in 1893, erected the genus SHlesia to accommodate the
two species described by Rivolta, whicb clearly could not be retained
in the genus Taenia. The type-species is 5 . He also
described a new species, viz., S. vittata, from the camel
55
In the same year Stiles revised the diagnosis of the genus as
follows : —
‘ Head with four suckers, but no hooks ; strobila broader than long. Two distinct
sets of testicles present in each segment, one on each side, but no testicles in the
median line. Eggs very small and with one shell. . . . The following points,
which may prove to be of generic value, have been established only for
S, globipunctata ; genital canals pass dorsally to the nerve and ventral canal, but
vent rally of dorsal canal. Egg-shell with two conical projections at opposite poles.’
In 1903, Wolffhiigel obtained another species ( 5 . hepatica) from the
bile ducts of sheep and goats in South and East Africa. The worm
was described as double-pored.
In 1907, Fuhrmann described a fifth species which, he stated, was
also double-pored, viz., 5 . sjdstedti, and at the same time he also
placed the genera Stilesia and Thysanosoma in a new sub-family
which he named Thysanosominae.
Ransom (1909) had doubts as to whether the genus Stilesia
should not be included, along with the other genera possessing
paruterine organs, in the sub-family Paruterininae, even though
species referred to the latter sub-family are, for the most part,
parasitic in birds.
Gough (1911) pointed out that all species which at that time were
included in the genus Stilesia possessed neither vitelline gland nor
shell gland. He also drew attention to the fact that none of the
species had double pores, and that 5 . centripunctata differed from the
other species in having four distinct sets of testes and a single uterus
in each segment, the other species possessing only two sets of testes
and a double (? T.S.) uterus in each segment. He accordingly erected
a new genus which he named Avitellina, to accommodate A. centri-
punctata, The two genera Stilesia and Avitellina were placed in a
new sub-family which he named Avitellininae. His definition of the
sub-family and of the two genera was as follows : —
‘ Avitellininae : Scolex without hooks with four suckers, segments short,
genital pores irregularly alternating. Testicles in two or four groups, marginal,
none in the middle field. A single ovarium, no vitelline gland, no shell gland ;
uterus single or double, eggs finally enclosed in a paruterine organ. Eggs in ovary
and uterus surrounded (and nourished) by nutritive cells. Oncosphere with two
envelopes.
Type-genus : Avitellina Gough, 1911. All known species inhabit ruminants ;
development unknown.
5 ^
Stiksia Railliet, 1893. Type-species ; StiUsia gkhipunctata (Rivolta), Raiiliet,
1893.
Head with four suckers, but without hooks. Strobila thin and narrow. Genital
pores irregularly alternate. , Segments broader than long. Two distinct sets of
testicles present in each segment, one on each si^e, but no testicles in the median
line. Ovarium on the pore side. No vitelline gland, no shell gland. Uterus double,
finally void of eggs, which are contained in egg pouches (paruterine organ). The
genital canals pass dorsally of the nerve and the ventral canal, and ventrally of the
dorsal canal. Eggs with two envelopes. Habitat : Intestine of sheep, goat and
dromedary, and bile ducts of sheep, goat, and South African wild antelopes (Africa,
India, Italy and France).’
We have, however, noted above that the uterus in this genus is
single.
‘ AviUllina^ nov. gen. Type species : Avitellina centripunctata (Rivolta).
Head with four suckers, but without hooks. Strobila thin and narrow. Segments
broader than long, flat in the proximal portion of the strobila, nearly cylindrical in
the posterior portion. Genital pores irregularly alternate. Four distinct sets of
testicles in each segment, one right and one left of each longitudinal canal, but no
testicles in the middle field. Ovarium nearer the pore side ; no vitelline gland, no
shell gland ; a single uterus. Eggs finally enclosed in egg-pouches (paruterine
organ). The genital canals pass dorsally of the nerve and longitudinal canals. Eggs
with two envelopes. Habitat : Intestine of sheep, Africa, Italy.’
Blei (1921) erected the genus Hexastichorchis for a parasite from
sheep, with the following characters : —
‘ Strobila small and relatively thick. Dorsal longitudinal excretory vessel
lateral to ventral vessel. Testes in six rows, four after the disappearance of the
dorsal vessel. Paruterine organs single. Adults in sheep.
Type-species: Hexastichorchis pintnerilSitif
There is reason to believe that the species is distinct, and referable
to the genus Avitellina.
Meggitt (1924) included in the sub-family Avitellininae Gough,
1911, the three genera Stilesia, Avitellina and Hexastichorchis.
Unfortunately in his key to the genera of Avitellininae, Meggitt
states that the testes are in two rows, four rows and six rows on each
side, in the above genera, respectively. This is clearly an error ;
the number of testes on each side is half the number given by
Meggitt.
Woodland (1927) re-defined the sub-family Avitellininae Gough,
1911, and the genus Avitellina Gough, 1911, as follows *: —
^Avitellininae Gough, 1911. Scolex unarmed, with four suckers. Segments'
very short and the immature segmented strobila exceeding the mature in breadth.
Genital pores marginal and irregularly alternating. Testes in two or four columns,
marginal, none in the middle field. Ovary is small, compact and amesially placed
on the poral side. No separate vitellaria or shell glands. The uterus is single or
bi-partite, and develops in its interior a paruterine organ.
Type-genus : Avitellina Gough, 1911.
57
AviuUina Gough, 1911. Strobila thin (save in the gravid region) and narrow.
Four columns of testes and a single uterus, with paruterine organ, in each proglottid.
Cirrus sacs always shorter than the vulvae in mature segments. Cirrus sacs on
right side of strobila usually dorsal to vulvae, and on the left side usually ventral
to them. Genital canals pass dorsally to the lateral nerve and the dorsal and ventral
excretory canals. Ventral excretory canals in the posterior half of the strobila always
very large (the two covering at least one-eighth of the total proglottid breadth).
Type-species : A. centripunctata (Rivolta, 1874).’
In 1928, Woodland erected a new genus for a species found in
Taurotragus oryx, which he placed in the sub-family Avitellininae ,
namely Anootypus, with the following characters : —
* Strobila thin (save in the gravid region) and narrow. A single paruterine organ
is present in each proglottid. Cirrus sacs equal in length to, or longer than, the
vulvae, and constantly situated anterior and dorsal to them. Genital canals pass
dorsally to the lateral nerve and the excretory canals. Dorsal excretory canals are
absent, and the ventral canals become reduced in size in the gravid region of the
strobila. A single layer of longitudinal muscles is present in the parenchyma.
Type-species : A. edifontaineous Woodland, 1928.’
A second new species, viz., A, ricardi Woodland, 1928, was also
referred to this genus.
In the same paper Woodland suggested, in a foot-note, that the
definition of the genera Stilesia and Avitellina might
* be amended by excluding the number of columns of testes as a generic character
and by including the presence of both dorsal and ventral canals and a double layer of
longitudinal muscles in the parench}'Tna as additional characters.’
It will be shown later that a double layer of longitudinal muscles
only occurs in certain species, and that the dorsal vessel is very
variable.
Baer (1927), following Fuhrmann, placed in the sub-family
Thysanosominae Fuhrmann, 1907, all those genera which had
previously been placed in the sub-family Avitellininae Gough, 1911.
He defined the sub-family Thysanosominae as follows : —
‘ Large worms. Genital pores double or single ; in the latter case they arc
irregularly alternate. Genital canals dorsal to excretory vessels or between them.
Testes very numerous or few, in a single field, or in two lateral groups. Female
genitalia in poral half of segment. Vitelline gland may be absent in which case
the ovary contains the nutritive cells. Uterus tubular, sometimes very long and
undulating. Paruterine organs present ; may be very numerous or single. They
each contain several eggs. Adults in rumiii'ants.
Type-genus : 7hysanosoma Diesing, 1835.’
The latter genus previously contained three species, viz.,
T. actinioides Diesing, 1835 ; T, giardi (Moniez, 1879), from sheep,
cattle, etc., and T, pygargi Cholodovsky, 1902, from Capreolus
pygargus.
Baer, however, limited the characters of the genus Thysanosoma
so that it contained one species only, viz., T, actinioides. He
erected two new genera, viz., (i) Ascotaenia, to accommodate
T. pygdfgif and (2) Helictometra, to accommodate T. giardi. He
defined the above three genera as follows : —
‘ thysanosoma Diesing, 1835. Worms of medium size ; posterior edges of
segments fimbriated. Two sets of genitalia in each segment. Genital canals pass
between excretory vessels and dorsal to the nerve. Testes very numerous, occupying
the whole posterior half of the segment between the two ovaries. No vitelline or
shell gland. Uterus a single transverse tube which becomes undulated and expels
its eggs into numerous paruterine organs. Adults in ruminants.
Type*species : thysanosoma actinioides Diesing, 1835.’
* Ascotaenia Baer, 1927. Worms of large size with indistinct segmentation.
Genital pores irregularly alternate. Genital canals pass dorsal to excretory vessels.
Testes situated on each side of the female sexual glands, limited laterally by the
excretory vessels. Female genitaha situated in the poral half of the segment.
Vitelline gland small. Uterus a transverse tube becoming sac-shaped. There
are eight to twelve paruterine organs, each containing several eggs. Adults in
mammals.
Type-species : Ascotaenia pygargi (Cholodovsky, 1927).’
‘ Helictometra Baer, 1927. Worms of large size. Genital pores irregularly
alternate. Genital canals pass between the excretory vessels and dbfsal to the nerve.
Testes disposed outside the excretory vessels forming two lateral fields. Female
genitalia situated in poral half of segment. Vitelline gland and shell gland both
rudimentary. Uterus an undulating tube almost filling the entire segment.
Paruterine organs very numerous, each containing several eggs. Adults in ruminants.
Type-species : Helictometra giardi (Moniez, 1879).
Baer further considers that the genus Hexastichorchis is
synonymous with the genus A vitellina and that the species H, pintneri
Blei, 1921, is synonymous with A. centripunctata (Rivolta, 1874).
It is to be noted, however, that in H. pintneri^ the relative positions
of the dorsal and ventral excretory vessels to each other is quite
different from that obtaining in any other genus in the sub-family.
The sub-family Thysanosominae Fuhrmann, 1907, according to
Baer, thus contains the following genera : —
(1) thysanosoma with one species.
(2) Avitellina with two species. Woodland, in 1927, described
= Hexastichorchis four other species.
(3) Stilesia with four species.
(4) Ascotaenia with one species.
(5) Helictometra with one species.
(6) Anootypus with two species.
It is decidedly uhfortunate that authors have utilised different
characters in defining the above genera. Thus Gough differentiated
the two genera Stilesia and AviteUina by the fact that in the former
S 9
genus the testes are in two rows, the genital canals pass between the
excretory vessels, and the uterus and the paruterine organs are
double in each segment ; whilst in Avitellina the testes are in four
rows, the genital canals are dorsal to the excretory vessels and nerve,
and there is a single uterus and paruterine organ in each segment.
Both Woodland and Baer differentiate their genera on characters
other than the above.
Baer's two genera Helictometra and Ascotaenia differ from the
other genera of the sub-family in having numerous paruterine organs
and also in possessing rudimentary vitelline and shell glands. The
two genera differ from each other in the following points : —
In Ascotaenia the genital canals pass dorsal to the excretory
vessels ; the testes are situated on each side of the ovary but internal
to the excretory vessels, whilst in Helictometra the genital canals pass
between the excretory vessels and dorsal to the nerve, and the testes
are in two lateral rows outside the excretory vessels.
The principal characters attributed to the genus A nootypns
Woodland, 1928, are : —
1. The cirrus sacs are anterior and dorsal to the vulvae.
2. The genital canals are dorsal to the nerve and excretory
vessels.
3. There is a single layer of longitudinal muscles in the
parenchyma.
It will thus be seen that the three workers in this group, Gough, Baer
and Woodland, base their classifications on different sets of organs
and different combinations of characters.
Certain anatomical details may now be considered.
I. Relation of the cirrus sac to the vulva. Woodland regards
‘the arrangement of the cirrus sacs relative to the vulvae as one of the most
important, and so far as we know, constant characters distinguishing Avitellina
from Stilesia (at least equal in taxonomic importance to the number of the paruterine
organs.’
It will be seen, however, that this character is less constant than
is supposed.
The cirrus sacs in Anootypus are said to be anterior and dorsal to
the vulvae ; they arfe definitely anterior and ventral in the case of
S:hepaticaA^ Gough finds that in 5 . globipunctata the cirrus sac is
ventral to the vagina ; he does not state whether it is situated
anterior or posterior, but he figures the one directly ventral to the
* And in S. vittata also.
6o
other. Woodland says that the cirrus sacs are invariably ventral to
the vulvae, in the genus SHlesia,
In Avitellina, Gough states that the cirrus sac lies ventral or
dorsal, anterior or posterior to the vagina. He gives figures which
‘show the sagittal section through about nine sections, passing through four cirri
and vaginae ; it will be seen that the utmost irregularity has been realised.’
Woodland attaches little importance to this observation and
remarks that,
‘ in all AviUllina species the cirrus sacs on the left side of the strobilus lie ventral
to the vulvae, and on the right side dorsal.’
In the same paper, he, however, quahfies this statement by
saying that the above arrangement obtains in the majority of cases.
He further averts that in A. centripunctata the sacs are always
anterior to the vulvae but only in mature proglottides. The position
of the vulvae with reference to the cirrus sacs is not known in the
genus Hexastichorchis. The relation of these genital ducts to each
other in the genus Avitellina clearly requires further investigation
before a definite conclusion can be reached.
2. Longitudinal Muscles. Gough states that in Stilesia hepatica
and S. vittata the longitudinal muscles are in two layers. He makes
no reference to the musculature in S. glohipunctata. From the
account given above of the muscular system of 5 . hepatica, it will
be noted that the longitudinal muscles in this species are in one
layer, not two, and the same is the case in S. vittata. Woodland
states that in A . centripunctata the longitudinal muscles are in two
layers, viz., a small sub-cuticula layer and a large layer in the cortical
parenchyma. No mention is made of the musculature in his species,
A. lahorea, A. sudanea and A. chalmersi, but in his figures of these
species the longitudinal muscles are shown in two groups. In the
two species of the genus Anootypus the longitudinal muscles are in a
single layer, as in S. hepatica.
3. Excretory Vessels. In Stilesia and AviteUina the large ventral
vessel is lateral to the small dorsal vessel, but in Avitellina the
dorsal vessel is often microscopic and in A. centripunctata, a worm
measuring up to 285 cm. in length, the lumen of the dorsal vessel
is almost obliterated at 40 cm. from the scolex. In Anootypus the
dorsal vessel is entirely absent, a condition not very diflermt from
that obtaining in A . centripunctata. It is curious and important to
note that in Hexasiichorchis Blei, 1921, the large ventral vessel lies
internal to the small dorsal vessel. This fact is of some importance
and it means that Hexastichorchis pintneri is, at least, a valid
species.
In Stilesia, the genital ducts pass between the excretory vessels
but dorsal to the nerve, whilst in Avitellina they pass dorsal to both
the longitudinal excretory vessels and nerve. In Anootypus the
dorsal excretory vessel is absent and the genital ducts pass dorsal
to the ventral excretory vessel and nerve. In certain new species,
shortly to be described, the genital ducts appear to run ventral to the
excretory vessels.
4. Testes, In Stilesia the testes are in two rows. In Hexasti-
chorchis they are said to be anteriorly in six rows, but the outer row
consists merely of one or two irregular testes present only in some
segments, and the testes are really in four rows. In Avitellina they
are also in four rows, but in A, lahorea Woodland, 1927, and
A. sudanea Woodland, 1927, the outer column of testes is only
one testis deep and they are absent in some segments, whilst in
other segments more than one testis may be found. In Anootypus
they are said to be in either two or four rows.
5. Uterus, This organ is single in Avitellina^ Anootypus and
Hexastichorchis ; Gough states that it is double in Stilesia, but as we
have seen elsewhere, both he and Stiles note that the two uteri are
connected by a duct, the inter-uterine duct which they are inclined to
consider as the median portion of the uterus. I have shown above
that it is single in each segment, and consists at first of a transverse
tube having a dilated lateral termination on each side of the segment,
and that later on the transverse tube atrophies, leaving the dilated
lateral extremities isolated.
6. Par uterine Organ, In Avitellina, Anootypus and Hexasti-
chorchis this organ is single ; in Stilesia it is double. In a new species
to be described shortly the organ is single and lateral, Gough writes :
‘ It is a question I cannot attempt to decide, >vhether the paruterine organ of Stilesia
and Avitellina is homologous to the paruterine organ of other cestodes, as where it
has been observed previously it has generally been held to arise outside the uterus.
I am retaining the name as being convenient and as referring to a more or less
well-known structure but without prejudice as to its origin in other species. The
paruterine organs of various cestodes may quite possibly be of different origin, and
may only be convergent structures, as Fuhrmann has shown that they can
arise independently in various unrelated genera.’
62
The following table summarises the principal characters of four
of the genera in question : —
Stilesia.
Avitellina.
H exastichorebis.
Anootypus,
Longitudinal
muscles.
In a single layer.
In two layers, viz., one
small sub - cuticula,
the other large in
cortex.
In a single layer.
A double layer
in neck
region only.
Excretory
vessels.
Ventral vessel
large and
external to
small dorsal
vessel.
Ventral vessel large and
external to micro-
scopic dorsal vessel,
which latter often
atrophies in anterior
Osn e-seventh of
strobilus.
Ventral vessel large
and internal to small
dorsal vessel, which
latter atrophies near
middle of worm.
Dorsal vessel
absent.
Cirrus sacs.
Ventral to vulvae
on both sides.
Ventral or dorsal, or
anterior or posterior
to vulvae (Gough).
Woodland states that
the sacs are always
anterior to vulvae ;
on right side dorsal,
on left side ventral.
Relation to vulvae not
known, but figured
ventral to vulvae.
Always anterior
and dorsal to
vulvae on
both sides.
Testes.
Two rows.
Four rows except in
some species where
the outer row is
absent in isolated
segments.
In four rows ; but
before dorsal vessel
atrophies occasion-
ally a single testis
lies external to it,
giving false appear-
ance of six rows.
One species
with four
rows, the
other species
with two
rows.
Genital
canals.
Between ex-
cretory vessels
and dorsal to
the nerve.
Dorsal to excretory
vessels and nerve.
?
Dorsal to
excretory
vessels and
nerve.
Uterus.
Single.
Single.
Single.
Single.
Paruterine
organs.
Double.
Single.
Single.
Single.
There
appears to
be no possibility
of securing uniformity in
deciding which characters are of specific and which are of generic
value, but to the writer it seems desirable to keep separate the genus
Stilesia mainly on the grounds that the paruterine organs are double.
63
whilst in Avitellina, Anootypus and Hexastichorchis they are single.
It has been noted above that Woodland considers that the relation
of the cirrus sacs to the vulvae is a point at least equal in taxonomic
importance to the number of paruterine organs. This is not quite
true and the desirability of utilising paruterine organs as a basis of
classification will be evident when it is realised that these organs are
easily seen under low magnifications, and sometimes even with the
naked eye, whilst on the other hand the position of the cirrus sac
with respect to the vagina, can only be determined after a large
number of stained transverse sections have been examined ; and
even then, as pointed out above, the relation of these organs to
each other appears to vary in at least some species. Further,
in species in which external segmentation is indistinct or absent,
it is often extremely difficult to determine in the absence of a head,
which is anterior and which is posterior. I do not know which of the
characters dealt with above are of greatest taxonomic value, either
singly, or in combination ; doubtless, opinions on this subject will
differ, but it is clear that paruterine organs provide a simple, easy and
efficient means of diagnosing the genera Avitellina and Stilesia.
From what has been stated above it will be obvious that
unfortunately four genera, viz., Avitellina, Hexastichorchis, Stilesia
and Anootypus, have been erected to accommodate about twelve
species of cestodes which are closely related and which differ from
each other in minor details only — details which appear to the writer,
for the most part, of specific value only. I therefore consider that
the genera Anootypus H exastichorchis^x^^y of Avitellina,
and suggest that the characters of the latter genus be modified to
accommodate Woodland's two species of Anootypus, viz., that the
genus Avitellina be considered as embracing all those species with a
single paruterine organ in each segment ; the testes being in two or
four rows.
I accordingly re-define the genera as follows : —
Stilesia Railliet, 1893.
Strobila thin and narrow ; outer segmentation apparently always
distinct. Longitudinal muscles always in a single layer in the cortex.
A single set of genital organs in each segment. Testes in two rows.
Cirrus sacs ventral and usually anterior to the vulvae on both sides.
Genital ducts pass between the excretory vessels and dorsal to the
64
nerve. Uterus single, but paruterine organs double, in each segment.
Parasitic in ruminants.
Type-species :—S. globipuutata (Rivolta, 1874).
AviteUina Gough, 1911.
Synonyms : — Hexastichorchis Blei, 1921.
Anootypus Woodland, 1928.
Strobila thin and narrow ; outer segmentation either distinct or
indistinct. Longitudinal muscles in a single layer in the cortex, a
second smaller layer of sub-cuticula fibres may also be present. A
single set of genital organs in each segment. Testes in two or four
rows. Circus sacs dorsal or ventral and either anterior or posterior
to the vulvae. Genital ducts dorsal to both excretory vessels when
two are present. Uterus and paruterine organ single in each segment.
Parasitic in ruminants.
Type-species : — A. centripunctatd (Rivolta, 1874).
We have noted above that Baer has re-united the two sub-families
Thysanosominae and Avitellininae into one sub-family for which he
retains the name Thysanosominae and which he has accordingly
re-defined. The following table summarises the characters ascribed
by Baer to the two sub-families Anoplocephalinae and Thysanoso-
minae, into which, together with the sub-family Linstowinae, he
divides the family Anoplocephalidae.
•
Anoplocephalinae.
1
T hysanosominae.
Genital pores
Double, unilateral, irregularly alter-
nate or absent.
Double or single, in latter case
irregularly alternate.
Genitalducts
Dorsal to both excretory vessels,
except in one genus where they
; pass between them.
Dorsal to both excretory vessels,
or between them.
Testes
Numerous, sometimes only two j
in a single field.
Numerous or few ; in a single
field ; not in two lateral groups.
Ovary ...
In poral half of segment.
In poral half of segment.
Vitelline and shell glands . . .
Present.
Present or absent.
Uterus
Tubular, sac- like, or reticular.
Tubular.
Paruterine organ ...
Absent.
Present,
It will be noted that the only essential point of difference between
these sub-families is the presence of a paruterine organ in the sub-
6s
family Thysanosominae. I agree with Baer in including in this
sub-family the following genera, the characters of which may be
summarised thus
I and 2. Stile sia and AvitelUna^ the characters of which I have re-described
above.
3. ^hysanosoma differentiated from all other genera of this sub-family by the
possession of a double set of genital organs in each segment ; in addition
numerous paruterine organs are present.
4. As cotaenia differentiated from other genera in the sub-family by the fact
that the testes are situated between the excretory vessels and do not
extend lateral to them ; further, they lie on each side of the ovary, the
latter organ being in the poral half of the segment. A vitelline gland
is present but is very small. As in Thysanosoma^ paruterine organs
are numerous but it differs from this genus in having a single set of
genital organs in each segment.
5. Helictometra, In its general morphology this genus resembles Stiiesia and
Avitellina. The genital organs are single in each segment and the
pores irregularly alternate. The genital ducts pass between the
excretory vessels and dorsal to the nerve. Unlike Stiiesia and Avitellina^
however, the testes in this genus are situated lateral to the excretory
vessels. It also differs from the latter genera in possessing rudimentary
vitelline and shell glands and very numerous paruterine organs.
The following key will serve to emphasise the outstanding points of
difference between the genera included in the sub-family : —
With a double set of genital organs in each segment ... T hysanosoma
With a single set of genital organs in each segment ... i
1. With one paruterine organ in each segment Avitellina
With more than one paruterine organ in each
segment 2
2. With two paruterine organs in each segment Stiiesia
With numerous paruterine organs in each
segment 3
3. Testes within the excretory vessels Ascotaenia
Testes in two fields, one lateral to the excretory
vessels on each side Helictometra
As indicated elsewhere, a further contribution will follow shortly,
and will deal with species of certain of the above genera.
ACKNOWLEDGMENTS
My thanks are due to Miss E. H. Michie and Mr. David Dagnall
(of the Liverpool School of Tropical Medicine), for the figures
illustrating this paper.
66
EXPLANATION OF LETTERING.
c.c, — calcareous corpuscles.
c,j. = circular fibres.
c. p. =: cirrus pouch.
d. c.v. — dorsal excretory vessel.
e. v. = excretory vessel.
g.a. = genital atrium.
l.m. = longitudinal muscles.
0, — ovary.
p.u,o, — paruterinc organ.
p.u.p. — paruterine pouch,
r. s=; testes.
u. = uterus.
t>. = vagina.
v. d. = vas deferens.
v.e.v. = ventral excretory vessel.
EXPLANATION OF FIGURES.
Stilesia bepatiea.
Fig. I. Outline of the transverse sections of two succeeding segments showing the relationship of
the vulva and the cirrus pouch. X 53*
Fig. 2. Transverse section of mature segment showing the musculature and male and female genitalia.
X 53 -
Flo. 3. — Outline of transverse section of mature segment showing transient uterus. X 53*
B. — Uterine tube more highly magnified. X 400.
Fig. 4. Outline of transverse section of mature segment showing atrophy of the transient uterine
tube.
Fig. 5. Gravid contracted segments showing uterus, paruterine organ, paruterine pouch and
(?) calcareous corpuscles. X 46.
Fig. 6. Gravid segments showing relationship of paruterine organ and paruterine pouch. X‘ 46.
Fig. 7. Poral side of segment showing paruterine organ and pouch. X 240*
Fig. 8. Poral side of segment showing paruterine organ and pouch in communication. X 240.
Fig. 9. Gravid segments showing (?) calcareous corpuscles. X 53 *
REFERENCES
Ba£r, J. G. (1927). Monographic des Cestodes dc la Famille des Anoplocepbalidae, Paris.
Blei, R. (1921). Drei neue Schafzestoden. Centrbl.f. Bakt.^ Grig., 87 , 365-
Gough, I.. H. (1911). A monograph of the tape- worms of the sub-family Avitellininaey being a
revision of the genus Stilesia and an account of the histology of Avitellina centripunctata (Riv.).
Qtuirt JL Microscop. Sci., 56 ^ 317.
• (*909)* The anatomy of Stilesia centripunctata (Riv.). Transvaal- Dept, Agric. Vet. Bad,
Lab.y p. 113.
Marotel, M. G. (1903). Contribution a Titude zoologique du Stilesia centripunctata (Riv.). Note
prdiminaire. Jl. Med. Vet. et Zootech.^ Lyons, 5 Sir., 7 , 24.
Stiles, C. W., and Hassall, A. (1893). A revision of the adult cestodes of cattle, sheep and allied
animals. U.S. Dep. Agric. Bur. Anim. Ind., Bull. 4 .
Woodland, W. N. F. (1927). On three new species of Avitellina (Cestoda) from India and the Anglo-
Egyptian Sudan, with a re-description of the type-species A. centripunctata (Rivolta), 1874.
Ann. Trop. Med. & Parasitol., 21 , 385. “
(1928). On a new genus of Avitellinine tape-worms from ruminants in East Africa.
Parasitol.f 20 , 56.
THE DISTRIBUTION OF BLACKWATER
FEVER IN AFRICA*
BY
J. W. W. STEPHENS
{Received for publication 13 February, 1929)
Abyssinia.
Two Maps
Locality
Cases
Authority
Dire-Daoua ...
I (1911)
PIchoy (1912), p. 617.
Algeria.
J.ocallty
i
1 i ases
i
Authority
General
Parrot (1915) states that
! almost all the foci are
situated in maritime or
juxta-maritime regions, at
the mouths of rivers or in
the valleys they drain — (i)
Seybouse and Saf-saf in the
East, Macta in the West ;
(2) the high plateaux ; foci
at Ain-touta, Batna Tiaret ;
(3) oases of the Sahara ;
(4) sporadic cases at Algiers,
Alma (Mitidja), Guyotville.
Parrot (1915), p. 29.
‘ Nous pouvons ^valuer a la
centaine la totalite des cas
connus, pour la piriode qui
va de 1899 a la fin de 1920.’
Parrot (1921).
‘ La fievre bilieuse h^moglo-
binurique tendait a prendre
une place importante dans la
pathologic des Europ^ens
d’Algdrie.’
loc. cit., p. 59.
‘ Parait extremement rare en
1912.’
Campagne (1913), p. 71.
• Stephens, J. W. W. (1927). The distribution of blackwater fever in Europe. Ann. *lTop.
Med. & Parasitol., 21 , 467.
(1928). The distribution of blackwater fever in South West Asia. loc. cit., 22 , 53.
(1928). The distribution of blackwater fever in India, loc. cit., 22 , 170.
(1928). The distribution of blackwater fever in Burma and the Far East. loc. cit.,
22 , 179 -
67
58
Algeria — continued.
Locality
Cases
Authority
D^partement
d ’ A 1 g e r —
Alger
1 (1906)
Sergent, Ed. and Et. (1907), p, 32.
Alma
{Plain of La Mitidja)
I (1910)
I (1914)
Parrot (1915), p. 29.
Bouira j
‘ Locality r6put6c depuis
longtemps comme tres palu-
ddenne et uu Ton constate
presque chaque ann^e des
cas de fi^vre h^maturique.’
Sergent, Ed. and Et. (1921), p. 330.
Guyotville
1 ( )
Parrot (1915), p. 28.
Maison-Carree
{near Algiers)
I (1901)
Brault (1903), p. 561.
D6partement de
Constantine —
Aln-touta {Mac-mahon)
‘ Des cas de fi^vre bilieuse
h^moglobinurique y sont
constates chaque ann^e.*
Anon (1923), p. 473.
... (1*917)
... (1918)
I (1919)
... (1920)
(Native) i (1921)
4 (1917-zi)
Parrot (1921), p. 60.
Parrot (1923), p. 607.
loc. cit.
Barral Guehar
2 (1905)
Sergent, Ed. and Et. (1911), p. I4r>.
Batna
‘ On y constate chaque <§t6 des
accis de fi^vre a forme
pernicieuse et des cas tres
graves parfois mortels, de
fievre bilieuse h^moglobinu-
rique.’
Anon. (1923), p. 432.
‘ Les cas d^accis femicieux et
de bilieuse hemoglobinurique
sont frequents dans ces
“ quartiers
4 (* 9 * 8 )
5 (• 9 > 3 )
Ballet (1923), p. 556.
Sergent, Ed. and Et. (1921), p. 330.
Campagne (1914), p. 25.
Duxerville
1 (1912)
Parrot (1915)) p. 29.
* ... Under the column < Cases signify that cases are recorded hut that the number is not
stated. This does not apply to the tables with eight columns.
69
Algeria — continued.
Locality
Cases
Authority
Department de
Constantin e — {contd .) —
EV~Arroucb
4 (1899-1908)
2 (1909)
7 (1910)
Several (191 1)
0 (1912)
Parrot (1915), p- 29.
Gudhar
Sergent, Ed. Correspondence.
Guelma
Parrot (1915), p. 28.
Mondvoi
{Adjacent Localities)
6 (1901-10) i
I (1905)
Several (1906)
(1907)
?I 9 o 8 )
(1909)
1 (1910)
3 (19*0
2 (1912)
2 (1910)
Parrot (19H;), p- 29.
Sergent, Ed. and Et. (191 1), p. 146.
idem (1914), p. 77.
Parrot (191 5) p. 29.
Sergent, Ed. and Et. (1914), p* 77*
Morris
1 (1908^
I (1920)
Parrot (1915), p. 29.
Sergent, Ed. and Ef. (1921), p. 331.
Otded-Rabmoun
» (^903)
Sergent, Ed. and Et. (1904), p. 324.
Pentbiivre ...
2 (1910)
Sergent, Ed. and Et. (191 1), p. 148.
Robertville
* Cas nombreux.*
idem^ p. 132.
Robertville ...
6 deaths (1909)
7 » ? (i9>c>)
3 ? (19*0
0 fi9i3)
0 (1914^
0 (19*5)
36 (18 years)
4 (1908-11)
32 (I91I-Z7)
Ciavaldini (1917).
Ciavaldini (1927).
Sey bouse f Valley of
4 ( )
Sergent, Ed. and Et. (191 1), p. 96.
Taber
2 (1921)
Anon (1923), p. 485.
Touggourt
X (1920)
Sergent, Ed. and Et. (1926), p- 331.
Department d’Oran —
Cbeliff Valley
...
Sergent, Ed. Correspondence.
Habra Plain
Macta Valiev
70
Algeria — continued.
Locality
Cases
Authority
Plain of the Mact a —
ArzcwtoAi n-T c d e I c s
Araev)
25 (1904-05)
Costc (1906).
Cassaigne
Parrot (1915), p. 28
Falikao
Campagne (1914), p. 52.
Sergent, Ed. and Et. (1915), p. 5.
Sehdou
4 (*904)
Claude (1905), p. 274.
7 iaret
Parrot (1915), p. 28.
7ourvilU
Sergent, Ed. Correspondence.
Angola.
Locality
Cases
Authority
Oenerol
8 deaths
Da Silva (1898, 1899).
Plehn (1899), p. 240.
Benguella
3 (1905)
Pinheiro (1906), p. 276.
1 (1910)
Barreto (1913)) p. 107.
Loanda
‘ Malaria in a great number of
cases took on a grave form, j
blackwater fever, and per-
nicious.'
Pinheiro (1906).
Mossamedes ...
5 (*9io)
Barreto (1913).
Mofambique ...
I (1910)
S.S. Beira 1
!
I (1912)
Basutpland.
Europeans
Cases
Deaths
...
Natives
..
j
Cases
Deaths
Year
Authority
1603
(year 1921)
No
records'
j
495»937
natives
1,241
Coloured
No
records
...
1926
I
" !
• i
Basutoland (1927).
BeCHUAN ALAND.
Locality
1 Cases
Authority
t
\ i {1927-28)
Bechuanaland Protectorate, p. 22.
71
Cameroons,
Europeans
Cases
Deaths
1
Natives
Cases
Deaths
Year
Authority
826
24
1903-04
Medizinal,
pp. 150, 159.
30
5
I 904-05
pp. 94, 1 12, 113.
896
+
31
9
(Syrian^
0
1905-06
PP- 143, I55 j 162.
85
19
I
I 906-07
pp. 101, no, 121,
127.
Military
32
4
I 907-08
pp. 221, 229, 237.
31
4
...
I
I
1908-09
pp. 172, 177, 180,
199, 245.
38
6
1909-10
pp. 250, 255, 2^8,
381.
28
I
2
I
1910- 1 1
191 1- 12
p. 467.
30
191 1-13
Steudel (1924). p. 33.
Cameroon
{French)
{Douala
Hospital)
8
‘ La plu
ancien
leur af
3
part de <
8 ou surmi
fection en
CCS malades, colons
enes, avait contract^
dehors de Douala.’
1923
Letonturier (1924),
p. 396.
Congo.
Locality
Cases
Authority
Mid^Congo State
* I have had considerable ex-
perience among patients
suffering from this disease —
over a hundred — all of
whom recovered.’
Banks (1900), p. in.
Congo
50 (or 40)
20 negroes from the Antilles,
20 Europeans engaged on
railway construction.
Plehn (1899), p. 239.
Stanley Pool
25
loc. cit.
Basin oj the Congo
18
Vcdy (1907).
Brasizaville
2 (1922)
Blanchard and Lefrou (1922),
p. 699.
4
Ringenbach (1915), p. 120.
Leop<ddville ...
16 (1899-00)
Campenhout and Dryepondt
(1901), p. 55.
12 (1900-01)
Broden (1906), pp. 8, 58.
25 (1902-05)
loc. cit., p. 8.
20
Houssiau (1919).
ID ^ -
Van Hoof (1924)
72
Dahomey.
Locality
Cases
Authority
‘ Sur les cinq Europ^ens qui
ont attaints de cettc
maladie en 1921, un ne
prenait jamais la moindre
dose de quinine.*
Gautier (1922)*
* Gouzien . . . pendant son
s^jour a Dahomey a traits
... 53 cas.*
Eritrea.
Locality
^ Cases
j Authority
1
Case
1
... ‘I have been informed that a
Professor Franchini (1929).
: few very rare cases have
been found in Eritrea in the
Correspondence.
Setit ... ...
...! region of Gasc and Setit.*
French Equatorial Africa.
Locality
1 Cases
Authority
Loango
7 (1887-1888)
Gros (1890), p. 47.
Gabon (French Equatorial Africa).
Locality
Cases
• Authority
General
* Anderer Ansichtist Calmette,
Mense (1899).
welcher in Gabun 1886-87
sich sehr haufig mit dem
Schwarzwa8serfiebec.zuLbes-
chaftigen hatte.*
-
73
Gambia.
Europeans
Cases
Deaths
Natives
Cases
Deaths
Year
Authority
IS*
3*
I
10,000
(African)
100
(Mixed)
1910
Gambia —
pp. 25, 32.
230*
4*
2
7^470
1911
pp. 18, 25.
230I
3*
...
7>470
1912
p. 40.
230I
0
7470
*9*3
p. 25.
230I
0
7»47o
1914
P- 39-
0
0
*9*5
jS
...
1916
p. 24.
0
I
1917
p. 25.
0
...
1918
p. 16.
2»
1919
P- *3*
3*
1920
P- 13-
238
2*
1921
PP- 55 *7-
205
jS
I
9>395
1922
p. 28.
210
6*
4
9-567
...
1923
P- 34-
218
5
2
9-741
1924
pp. 6, 7, 8, 26.
2
1
I
1
1925
pp. 16, 17.
5*
2
1926
pp. 22, 45.
*7
3
1927
pp. 5, 22, 32, 46.
'ij Apparently refers only to Bathurst (Gambia),
[z) Apparently all European cases.
Gambia — continued.
Locality
Cases
Authority
MacCarthy Island {Gambia)
I (1910)
Gambia, p. 37.
(About 126 miles up the
River Gambia)
1 (1914)
p. 39-
« (19*7)
1
p. 26.
74
Gold Coast. ^
Europeans
Cases
Deaths
Natives
Cases
Deaths
Year
Authority
436
2
...
...
2
1893
Gold Coast (1894) —
pp. 25, 26.
769
C2*
5
I
I
1895
(*897), pp. 12, 14,
* 5 ) 24 *
798
...
...
...
...
...
1896
(1897), pp. 12, 21.
...
...
...
...
1897
...
...
...
...
...
...
1898
...
2
...
...
1899
(1909), p. 16.
5
...
...
1900
loc. at.
8
...
...
1901
loc. cit.
1,830
9
4
...
1902
loc. cit.^ pp. 7, 16.
1,796
8
6
...
...
...
1903
loc. cit.
1)953
*5
3
...
...
1904
loc, cit.
1,911
- *9
2
...
...
1905
loc. cit.
1,765
22
3
...
...
1906
loc. cit.
>.«77
27
4
...
...
...
1907
loc. cit.
1,768
21
7
...
...
...
1908 '
(1909). P- 43 *
1 ) 7*5
*7
3
...
1909
(19101, p. 6.
1,692
20
5
...
...
...
1910
(1911), pp. 9, 1 1, 39.
(1912), pp. 7, 9, 39.
2,245
8
2
...
...
1911
2,367
*4
6
...
...
...
1912
(1913I, pp. 10, 13.
2,590
21
5
...
...
1
* 9*3
(1914), pp. II, 13,
56, 62.
2,64s
21
5
...
...
...
* 9*4
(1915), pp. 13, 15,
(1916), pp. 10, II,
3 '. 35 -
2 ,CX 56
9
2
...
...
* 9*5
2,001
16
3
...
...
...
1916
(• 9 « 7 ). PP- 9 > 101 ^ 3 -
2,172
24
8
...
...
* 9*7
pp. 8, 10, 30.
>. 8*3
*7
4
...
...
...
1918
pp. 21, 40.
3 .« 8 i
14
7
...
6
I
* 9*9
(1919), pp. 7, 8, 10.
2,818
36
7
...
...
1920
(' 9 *>)> PP- 8, 34 -
(1922I, pp. 9, 32.
2 J 939
21
9
...
...
...
1921
2,901
48
6
...
...
1922-23
(1923), pp. 8, 61.
3,043
21
7
...
...
...
1923-24
pp. 8, 46.
3,104
16
2
...
...
...
1924-25
pp. 7. 38.
3)104
*3
5
...
S’*
2
1925-26
PP- 7 . > 0 . 34 -
3,481
7
3
...
...
...
1926-27
pp. 14. «05-
(ij The G0I4 Coast includes Gold Coast Colony, Ashanti and Northern Territories.
(2) Whether fion-official European cases have been recorded is not evident. The 12 cases include
3 deaths — ^haematuric fever (1), haemorrhagic fever (i), and hacmoglobinuric fever (i).
(3) 2 African.
75
French Guinea.
Locality
Cases
Authority
Conakry
1 (189s)
‘ De cettc observation et des
nombreux cas analogues ....
a Condkry.’
Maclaud (1895).
9
Le Moal (1905).
6 (1920)
Pelletier and Quemener (1921).
8 (1904)
Le Moal (1907), p. 258.
Boke
14 (1904-05)
loc. cit.
Conakry
Dakar
Conakry
73 (Aug., 1900-Mar., 1904)
Pinard and Boye (1904), p. 493.
Railway
12 (Aug., 1900-Mar., 1904)
Ballay Hospital
16 (1899)
. 14 (1900)
8 (1901)
10 (1902)
14 (1903)
62
Railway
2 (1910)
Savignac (191 1), p. 474.
Siguiri {Haut Nitfer)
6
Quennec (1895).
■
Quennec (1899).
[voRY Coast.
Locality
Cases
Authority
Grand Bassam
Haut SassandrUy Daloa and
Soubre
2 (1895)
6 O911-13)
‘ La fi^vre bilieusc hemo-
globinurique a 6t6 observ^e
a Daloa et a Soubr6, aussi
bien au d^but du sdjour
qu'apr^s plusieurs annecs
de presence a la colonic
mais toujours chez des
impalud^s.'
Crosse (1899), p. 120.
H^brard (1895).
Sorel (1913).
Blanchard fiqi i).
Abidjan ...
Bassam
Labou
Toun^i
4 Europeans
*3 »»
7
Vi vie (1907).
26 (1905)
76
Kenya (formerly East Africa Protectorate).
Europeans
Cases
Deaths
Natives
including
Asiatics
Cases
Deaths
Year
Authority
3.656
...
...
1911
East Africa
Protectorate-
4,9*3
14
...
1912
p. 52.
6.7*3
5
2
10
3
*9*3
pp. 28, 31, 118, 121.
7»297
II
3
...
9
I
*9*4
PP- 74, 77*
...
*5
4
4
I
*9*5
PP* 74, 77*
16
I
4
I
1916
pp. 64, 67.
... '
3
0
...
*5
5
1907
PP* 74, 77*
2
I
16
5
1918
PP* 7*, 75, 76.
29
8
11
4
*9*9
pp. 82, 83.
...
4
2
9
2
1920
Kenya, pp. 92, 93.
9.651
12
I
...
16
4
1921
pp. 128, 129.
18
3
21
7
1922
pp. 120, 121.
8
2
20
4
*923
pp. 84, 85, 86,
8
4
*3
5
1924
pp. 66, 71.
*5
5
35
10
*925
pp. 86, 96.
21
6
...
34
10
1926
pp. 72, 77, 82, 84.
*7
3
...
18
5
*927
PP* 52, 57, 62, 67.
72.
Kenya — continued.
Locality
Cases
Locality
Cases
Authority
Eliama Ravine ...
2
1913-1927
Kakamega
3 '
East Africa
Elder et
14
Kilindini
10
Protectorate.
Kenya.
Ewbu
I
Kidi
3
Fwt HaU
*5
KUmayu ...
2
Kacbeliba
5
Kisumn ...
6s
77
Kenya — continued.
Locality
Cases
Locality
Cases
1
j Authority
Kitui
6
Mumias ...
5
1 Kenya
Lamu
3
Nairobi ...
96
J^zvar ...
5
Nakuru ...
>3
Machakos
3
Narok
M'jerich
3
Northern Takana
2
Makindu
5
Nyeri
2
Malindi
3
Serenli
3
Meru
3
Voi
16
Mombasa
1 16
Tonte i
1
I
Mueressi
S
. -
4*3
These figures could only be used for comparative purposes if the population (European) of the
various localities were known.
Libya.
Locality
Cases
Authority
Tripolitania and Cyrenaica
‘ There are no cases of this
Professor Franchini (1929).
disease in the Italian North
Africa where malaria is very
Correspondence.
j rare.*
Morocco.
Locality
Cases
Authority
Gbarb District
I (1922)
Vialatte (1922).
Retbat
I (1925)
Vialatte (1925).
78
Nigeria.
Locality
Cases
Authority
Benin
*7
Giraud (1891), p. 406.
Nigeria, Northern.
Europeans
Cases
Deaths
Natives
Cases
Deaths
Year
Authority
21
S
1898
Nigeria, Northern
(1907).
22
3
00
loc. cit.
165
12
3
...
1900
loc. cit.
*65
rzi
I
1901
loe. cit.
0
0
20^
5
iyo2
he. cit.
309
17I
8
1903
loc. cit.
322
35 ^
6
1904
he. cit.
342
1 81
4
1905
loc. cit.
347
2^1
5
1906
he. cit.
424
12
0
6
I
1907
he. cit.
499
H
4
...
1908
Nigeria, Northern.
544
»3
3
2
0
1909
637
9
2
I
I
1910
' 641*
12
6
9-27 X !©•
I
0
191 1
pp. 4, 40.
703
*4
4
1
1912
pp. 7, 28.
804
17
4
1
1
...
19*3
p. 6.
969
22
...
1914
897
22
4
19*5
p. 23.
762
22
8
9
4
1916
PP- 301 35 -
779
*9
4
2
0
1917
pp. 153, 158.
989
27
7
' -
...
1918
pp. 37, 42.
ji) The fig:ure8 include non-Eutopean*.
[z) Not including 79 Lagos Railway officials.
79
Nigeria, Southern.
Europeans
Cases
Deaths
Natives
Cases
Deaths
Year
Authority
533
Z
1905
Nigeria, Southern.
21
4
1906
57
10
1907
i,244
48
8
oc
0
pp. 143, 150.
29
10
1909
(1912), pp. 62, 126.
34
7
1910
(1912).
1,648
25
8
I
I ?
1911
...
21
3
2
1912
1,589
26
6
8*1 X lo*
3
0
19*3
20
5
1914
1,650
r I
2
7
2
1915
pp. 42, 76, 80.
1,650
*9
4
8 1
*
1916
pp. 8, 46, 51.
1,650
22
11
5
2
1917 !
pp. 12,21,45^ 50*
29
4
0
1918
p. 20.
(i) African.
Nigeria.
Europeans
Cases
-
Deaths
Natives
Cases
Deaths
Year
Authority
...
38
10
3
0
19191
Nigeria (1919-21),
P- 73-
...
33
8
6
0
1920
41
10
5
*
1921
28
2
4
*
1922*
pp. 7, 64, 70.
25
6
II
8
1923
PP- 6, 49, 55-
24
12
7
0
1924
pp. 7, 12.
4,050
30
7
5 '
0
*925
pp. 12, 43, 49.
4,833
30
8 1
4
I j
1926
PP-45* 55-
5,493
31
5
»5
3
1927
P- 5.5-
S Northern and Southern Provinces combined (1919-21).
The returns for the year 1922 and onwards are for the combined Colony and Protectorate
of Nigeria, including that portion of the Cameroons now under British mandate.
8o
NyAS ALAND.
Europeans
Cases
Deaths
Natives
Cases
Deaths
Year
Authority
608
1905-06
NyasaYand.
583
1906-07
587
1907-08
595
»4
3
1908-09
pp. 5, 26, 27.
587
3
3
1909-10
5
3
1910-11
pp. 5, 10, 18.
4^
I
I
I
1911-12
P-5-
(Asiatic)
(1913), p. 10.
758
lO
I
1912-13
(Europeans
(Asiatic)
and Whites)
6
I
19*3
(1914), p. 12.
...
3
1
1914
(1915), p. 12.
2
1915
(1916), p. 10.
2
I
1916
1 (1918), p. 10.
2
I
1917
(1919), p. 9.
I
1918
(1919), p. 12.
6
1919
(1920), p. II.
*’*55
1 1
I
1920
(1921), p. II.
H
2
1921
(1922), p. 12.
(Europeans
and Whites)
H
6
1922'
(1923), p. 10.
13
2
...
I
0
1923
(1924), p. 9.
(Asiatic)
5
2
1924
p.8.
3
3
I
*9^5
p. 7.
3
0
*8
1926
p. 7.
II
2
3
1927
p. 7.
(i) II in 1912-13 Reporl.
Portuguese East Africa.
Locality
Cases
Authority
Angoche
‘ Mortality : ten times greater
Soromenho (1923).
Cbinde ...
than the mortality for
Jnhambane ...
malaria.*
Lourenfo Marques ...
Mozambique
Quelimane
Tete
Mozambique T erri tory
* Blackwater fever is the disease 1
Turner (1910), p. 112.
Delagoa Bay
Ayhich causes more anxiety
than any other to the
European population of the
whole territory of Mozam-
bique.*
7
Garin (1910), p. 252.
Rhodesia, Northern.
Europeans
Cases
.1
Deaths
Natives
Cases j
Deaths
Year
Authority
4,600
(35)'
7
1,140,642
(Africans)
1925
Rhodesia, Northern
(192813), pp. 20, 21.
(6o)i
12
1926
he. cit.
1
29
9
1
!
1927
Rhodesia, Northern
(1928ft), pp. 13, 39,
42, 45, 48, 74-76.
(i) Cnses estimated on a basis of 20 per cent, mortalit)’.
Rhodesia, Southern. ^
Europeans
Hospital
Cases
Deaths
Natives
Cases
Deaths
Year
Authority
...
73
‘7
1
1
1906
Rhodesia, Southern
(1908), p. 15.
14,007
13
1907
(1908), p. 15.
14,640
41
12
1908
(1909), p. 19.
75
18
3
I
1909
(1910), p. 15.
75
17
I
1910
(191 1), p. 16.
39
7
1
191 1
(1912), p. 24.
60
17
1
1912
(1913), p. 22.
57
14^
4
1913
(1914), pp. 31, 34.
53
13*
0
1914
(*9*5)7 PP- *77 30-
60
16*
2
* 9*5
(* 9 * 6 ), pp. 24, 27 -
34
5
•
1
1916
(1919), p. 29.
48
13
1917
loc. cit.
...
32
10
4
1
1918
loc. cit.
(i) Southern Rhodesia includes Mashonaland and Matabelcland.
(*) 34 j P‘ 34 * (3) European deaths 28, Indians i, pp. 30, 31. (4) 37, p. 27. Natives 2 deaths, p. 28.
g2
Rhodesia, Southern — continued.
Europeans
Hospital
Deaths
Natives
Cases
Deaths
Year
Authority
Cases
Rhodesia, Southern
38,284
36
I
1919
(1920), pp. 29, 32.
70
10*
5
0
1920
(1921), pp. 30, 33,
34.
33,620
53
6*
...
...
1921
(1922), pp. 7, 39,40.
49
*4
I
1922
(*923)1 p. 36.
...
64
14 M
...
1923
(1924), p. 19.
—
122
40 T
)
...
20
I H
1 -
3
2
1924
(*925)1 pp. *^i 50,
...
39
II T
53-
...
52
13 H
1925
(1926), pp. 16, 42,
...
78
26 T
43.
37
II H
1 -
1926
(*927)1 pp. 21, 7.I1
...
21 T
J
77, 80.
36
13 H
) -
I
I
1927
(1928), pp. 47, 70,
) ...
72i 74i 78-
...
15 T
I
(1) European deaths 9 (1916), 17 (1917), 17 (*9*8), *8 (*9*9).
Native deaths o (*916), o (*917), * (*9*8), * (*9*9)-
The figures for total European deaths from Blackwatcr do not agree with those given in
earlier reports.
(2) Europeans 22 deaths, Natives 2 deaths, pp. 33, 34.
(3) Europeans 23 deaths, Natives i death, pp. 39, 43.
H — hospital cases, t = total cases.
Senegal.
European cases
Deaths |
Native cases |
Deaths |
Year
Authority
22
5
* 9 QS
Merveilleux (*9x0),
P. 693.
44
6
*906
27
5
...
1907
50
8 1
j
1 1
1
t
1908
45
12
...
;
1909
83
S E N ECAL — continued.
■t--
Locality
Cases
Authority
General
I (1925)
Huchard (1925).
Bakel
Barth^lemy-Bcnoit (1865).
Dagana
loc. cit.
Didtar
6 (1909)
Ros^ (191 1).
‘ a Dakar les cas sont frequents.’
Dakar
Esquier (1922).
{d Vinfirmerie du Marisoi)
European
and
Black-
Native Malaria water
Strength. Cases. Cases. Year.
204
187
0 191 1
232
247
4 1912
291
206
II 1913
387
229
1 1914
349
291
5 I9C5
363
409
0 1916
495
71 1
I 1917
L103
1,780
II 1918
770
846
16 J919
4 (1914-16)
Marcandier (1916).
Cases
Deaths
Year
Dakar
IZ
6
1892 -1894 Clarac (1898).
24
6
1894 1896
33 (1909)
Merveilleux (1910), p. 689.
Kaslack
3 deaths (1926) Dupont (1928).
Keniiba
I Barth <^lemy-Benoit (186^).
{abandonne depuis i86i)
1 . .
Midine
00
<.n
00
1
OC
'sO
Cases
Deaths
Year.
St. Louis
3
2
1857 loc. cit.
(a Vhdpital de)
9
4
1858
4
2
1859
II
2
i860
II
5
1861
26
3
1862
24
7
1863
I (1911)
Gastou and Dufouger^ (1911),
p. 301.
9 (*909)
Merveilleux (1910), p. 689.
Cases.
J^caths.
Year.
Goree Islands
I
...
(1855) Barth 61emy-Benoit (1865).
I
(1856)
2
(•857)
8
(1858
6
('*59)
4
I
(i860)
12
3
(1861)
35
10
(1862)
39
8
(1863)
‘ depuis vingt ans —
. a Gor6e B^renger F6raud (1874), p. 62.
285 bilieuees h^maturiques |
9ur pr^s de 23 mille entries.’ 1
* (*909)
Merveilleux (1910), p. 689.
Saint Louis Island
‘ depuis vingt ans nous voyons B^renger F^raud (1874), p. 61.
qu’il
y a eu a Saint-Louis,
178 fievres bilieuses m^Ianu-
riqucf
seulement, sur pr^s de
43 mille entries i Thfipital.’
84
Sierra Leone.
Europeans
Crises
Deaths
Natives
Cases
Deaths
Year
Authority
620
5
I
1909
Sierra Leone, (1910),
831
12
4
1910
PP- 6 , 54, 69-
(1911), pp. 6, 24,
(Europeans
and Whites)
, 2
I
1911
49, 60.
(t9i2), pp. SI, 57.
8
4
1912
(i 9 i 3 )> PP- 7 , 43 . 30-
9
2
1913
(' 9 ' 4 )- P’ 5 -
...
11
4
1914
P' 5 -
...
6
0
1915
p. 7.
‘,138
3
0
1916
pp. 14, 26.
'3
I
1917
PP- ■ 3 > H, 33. 38.
1,036
I
...
1918
pp. IS, 40.
1,176
6
1919
pp. 8, 42.
6
...
1920
p. 38.
6
T921
(1922), p. 43.
...
6
3
1922
(>923). P- 39 -
5
I
I
1923
(1924), pp.9,35,42.
5
I
2
1924
(1925), pp.9,37,44.
3
2
...
1925
(1926), pp.6,34,41.
4
I
3
I
1926
(' 927 )iPP- 6 . 3 >, 38 -
...
4
2
...
5 ^
4
1927
(1928), pp. 6, 42, 55.
(i) I African.
85
Somaliland.
Locality
Cases
Authority
Protectorate, British
‘ I have seen one patient who
seems to have suffered from
the disease in Somaliland.’
Crosse (1899), p. 114.
No records (1923-1927)
European
Population. Natives. Year.
52^ 300,000 1927
Somaliland Protectorate.
Italian
‘ One mortal case was reported
by one of the doctors of this
Institute (Or. Martinelli) in
1926, in the region of Lugh.’
Professor I'Vanchini (i92<)).
Correspondence.
‘ Another doctor of this Insti-
tute, Dr. Veneroni, in 1924
reported two cases among
the white men in the
English Jubaland, which is
now an Italian possession
(the Oltrcgiuba).’
‘ La febbre biliosa emoglo-
binurica nella Somalia
Jtaliana c forsc mcno rara
di quanto si sarebbe indotti a
giudicare dalla deficienza
di comunicazioni nosogra-
fiche e anche da qualche
asserzione negativa a
riguardo.’
Cosinto (1927).
(i) 72 including Air Force.
Sudan (Anglo-Egyptian)
Locality
Cases
Authority
Atbara
I (1926)
Anon (1928).
Babr-el-Ghazal
2 (1905)
10 (?)
‘ Blackwater fever is certainly
more common .... in the
Bahr-el-Ghazal than in
some of the districts of the
White Nile.’
Ensor (1906).
Mongolia
I (1926)
Anon (1928).
Roscires {Blue Nile) ...
* A notoriously malarial station
where blackwater fever is
known to occur.’
Balfour (1913), p. 37.
f$^au
3 deaths (1905)
Wenyon (1928) (personal com-
munication).
86
Sudan, French.
Locality
Case#
Authority
Bamako {on the Niger)
Rousseau (1887).
Kati
17
Cardeillac (1905).
Bakel
Bammako
Faboulabe
Kayes
Kita
Niagassola ...
Siguiri
Campagnc du Soudan,
1889-1890
Cases Deaths
10
4 1
3 2
9 2
I I
1 I
Durand (1891), p. 15.
29 7
‘ Nous devons done nous con-
tenter de comprendre dans
ce groupe de fi^vres bilieuses
r^mittentes la m^anurique
et Th^maturique en faisant
toutefois observer que la
premiere cst bien plus
fr^quente que la seconde.’
Bamako
2 (1896)
Carmouze (1897).
Djcnne
. (.896)
Kayes
18 (1895-1896)
Kita
I (1896)
Siguiri
I (1896)
T ous Ics posies du Soud an ...
Deaths Year
II (*889)
II (1890^
13 (1891)
16 (1892)
25 (>893)
25 (1894)
7 (>895)
8 (1896)
Dakol ...
2
Henric (i^8).
Kankan
I
Quennee (1899).
Kita
i
i
00 j
87
Tanganyika Territory (formerly German East Africa).
Locality
Cases
Authority
23 (1894-95)
Mann (1902).
32 (
; i 895 - 96 )
19 (
1896-97) !
30 (
[1897-98)
32 (
[1898-99)
Tanganyika Territory.
Europeans
Cases
Deaths
Natives
Cases
Deaths
Year
[
Authority
30
3
4,107,000
12
4
1921
Tanganyika Territory,
p. iir/.
44
4
3
1922
pp. 63, 108.
19
4
16
3
1923
(1924), p. 138.
16
2
i
3
1924
p. 138-
7
8
1925
pp. 10, 13.
»5‘
10
4,319,000
9
1926
(1927), p. 15.
72*
6
10
1927
(1928), pp. 14, 19.
(i) Total number of cases. How many European cases is not evident.
ss
Tunis.
Locality
Cases
Authority
‘ Cette maladie n’y a jamais 6 t 6
constat^e de fa^on certaine.’
Gouzien (1911).
Nicollc, C. (1929). Correspondence.
Uganda Protectorate.
Europeans
Cases
Deaths
Natives
Cases
Deaths
Year
Authority
10
2
(total)
1904
Uganda Protectorate
(1918), p. 12.
14
3
(total)
1905
4*
4
(total)
1906
10
2
(majority
Asiatics)
1907
1908 Report type-
script.
13
2
1908
1908 Report type-
script.
...
21
6
(total)
1909
(1918), p. 12.
26
6
(total)
1910
he, cit.
4
I
14
2
191 1
(1913), p. 10.
10
4
2,840,469
35
5
1912
(>9*3), PP- >0, 17.
<S23
2
2,889,561
39
10
1913
(>9>4), PP- >2, >9-.
1,017
28
8
2,904)454
54
13
1914
(1916), pp. u, 17.
^5
18
(total)
1915
(1916), p. 9.
46
10
(total)
1916
(1917), p. 8.
8
2
4*
6
1917
(1918), p. 12.
40
7
I (total)
1918
(1921), p. 43.
894
24
4
59
H
1919
loc. cit.
942
12
*
44
6
1920
loc. cit.^ pp. II, 44.
12
3
!
501
12
1921
(1922), Appendix.
' *5
4
68*
10
1922
(1923), Appendix.
10
3
6i«
14
1923
Appendix, p. 97.
10
2
61
21
1924 .
(1925), Appendix,
, P- 57-
10
3
71
19
1925
(1926), Appendix,
p. 67.
21
2
150*
48
1926
(1927), Appendix,
p. 61.
20
6
i
86
22
1927
(1928), Appendix,
P- 75-
(1) 49 Asiatics, i African. Europeans ii cases, 3 deaths. Asiatics 72 cases,
(2) 67 Asiatics, i African. 14 deaths, p. 96.
(3) Asiatics. (4) 127 Asiatics.
89
Union of South Africa.
Locality
Cases
Authority
Union of South A frica
1 . Cape of Good Hope
Province.
2. Province of Natal.
3. Province of Oranf^e Free
State.
4. South West Africa
Protectorate {mandated).
= German South West Africa.
5. Province of Transvaal.
No records (1927)
Population : —
Europeans ... 1,637,472
Bantu 5 ?c» 34 i 5 h 3
Asiatic ... 172,577
Mixed ... 563,320
7,407,932
Union of South Africa (1927).
Cape Province
(— Cape Colony)
‘ There is no blackwater fever
in Cape Colony.*
'rurncr (1910), p. 111.
Natal
‘ It has, though exceptionally,
been seen.’
‘ riierc have, however, been
two or three cases in the last
four years reported as black-
water fever in persons who
certmnly contracted the
disease in Zululand or in
Natal, close to the river
Tugela.’ (Hill.)
Clenunv (1903), p. 47.
Turner (1910), p. 1 1 2.
South-West Protectorate
{formerly German South 1
West Africa)
II (1894-95)
5 (1907-08)
I (1910-11)
(Europeans ... 10,456
Natives ... 33,344)
1 Mann (1902).
Medizinal, pp. 309, 314.
loc. cit.
Transvaal* ...
‘ In the northern portions of
the 'I'ransvaal such as the
Zoutpansberg and Water-
berg districts, it is also
prevalent.’
'rurner (1910), p. 112.
Zoutpansberg District . . . i
‘ Since 1896 the cases have
followed one another very
quickly and I reckon that
there arc on the average
five to ten cases a* year in
this part of the district
where the population is
small and much scattered.’
Boric (1911), p. 239.
• Transvaal and Zululand. — Dr. W. A. Murray, of Pretoria, in a letter says : — ‘ It is relatively
common in the Lowveld of the Transvaal ; at Komatipoort alone there had been eight or nine
cases in 1926.’ ‘ In certain areas of Zululand it is equally common.’
90
West Africa.
Locality
Cases
Authority
* Tableau de la frEquence
proportionelle des maladies
endemiques dans les diverses
possessions fran^aises de la
cote occidentale d’Afrique
(rapportE au dEnominateur
de 100 hommes et d’un an).
BErenger FEraud (1874), p. 238.
FiEvre mElanurique.
Cases Deaths
Gorce
3*03 -91
St. Louis
0*93 *28
t /5
Moyen .;.
3*90 1-24
Haut
21-31 4-26
Cay or
77* ai-33
Rivi cres de Sud
14-86 3-39
(Cazamance, Rio Nunez)
Cote d'Or
37-70 4-01
1
Gabon
1
1 53*05 3*8o
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(b) ‘ Annual Report on the Medical and Sanitary Departments for the Year ended .’
(c) * Annual Medical and Sanitary Report for the Year ending
(d) * Annual Medical and Sanitary Report for the Year — —
(e) * Annual Medical and Sanitary Report — —
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Sierra Leone. Annual Medical Report* for the respective years.
Somaliland Protectorate. Annual Medical Report* for the respective years.
SoREL (1913). Traitement dc la fievre bilieuse h^moglobinurit[ue par ies injections et lavages di'
solutions sucrees. Ann. d'hyg. et de med. col.., 16 , 194.
Soromenho, L. (1923). Epidemiology of malaria and blackwater fever in Portuguese East Africa
between 1901-1920. Med. Jl. of South Africa, 18 , 201.
Steudel, E. (1924), Aus den Jahres-medizinal Berichten, 1912-13, der tropischen Deutschen
Schutzgebiete. Arch. f. Schijfs.- u. Prop. Myg., 28 , Beiheft, i.
Tanganyika Territory. Annual Medical Report* for the respective years.
Turner, G. A. (1910). A resunid of the literature of blackwater fever. Transvaal Med. JL, 5 , 1 t i.
Uganda Protectorate. Annual Medical Report* for the respective years.
Union of South Africa. Annual Medical Report* for the respective years.
Van Hoof, L. (1924). Spirochetes dans des acces de bilieuse hemoglobinurique chez dcs Europi^ens
au Congo beige. Bull. soc. path, exot., 17 , 291.
Vedy, L. (1907). La fievre bilieuse hemoglobinurique dans le bassin du Congo. 8°, 152 pp. Bruxelles.
Henri-Lamertin, librairie-editeur.
ViALATfE, C. (1922). Le paludisme au Maroc. 6pidcmiologic-Prophylaxie. Arch, de V Instil. Pasteur
de VAfrique du JNord, 2 (4), 609.
Syndrome bilieux-hemoglobinurique au cours d’un acces de paludisme. Bull.
soc. path, exot., 18 , 715-
ViviE (1907). Etat sanitaire et maladies observees a la Cote d’Ivoire pendant I’annee 1905. Ann.
d'hyg. et de mid. col., 10 , 119.
94
ISLANDS
Cape Verde Islands.
Locality
Cases
Authority
Saint-Nicolas
‘ Quant 4 la fievre bilicuse
h^moglobinurique affection
parapalud^enne, on la ren-
contre quelques fois k Saint
Nicolas (Riberia - Brava)
tris rarement dans les autres
lies.’
Fatome (1907), p. 246.
Comoro Islands.
I.ocality
Cases
Authority
General
' La bilteuse h^maturique
s'observe commun^ment.’
Fontoynont (?), pp. 258, 263.
Mayotta
Le Roy de M^ricourt (1853).
‘ At Mayotta in the Comoro
Islands itis very prevalent.’
Clemow (1903), p. 47.
Lafont (1908).
...
Gouzien (191 1).
i
‘ C’est encore chez les creoles
que se d^veloppe le plus
friquemment la fievre
bilicuse h^moglobinurique.’
‘ La fievre bilicuse hemoglo-
binurlque pr^sente chez les
Europ^ens des caracteres
tris diffirents.’
Blin (1905).
I
Vaysse (1896), p. 234.
MohHi
2 (1903)
‘ I.a fi<ivre bilieuse h^rao-
globinurique est rare et peut-
etre faut-il attribuer cet
raret^ au nombre rcstreint
de blancs. Cependant deux
cas suivis de d^c^s sont sur-
venus en 1903. Ce sbnt les
deux premiers cas ob^rv^
au cours des dix dernieres
ann^k*
Lafont (1,905), p, 51 1.
95
Conakry.
m
Locality
Cases
Authority
vide French Guinea
Fernando Po.
Locality
Cases
Authority
Fernando Po
‘ Die chinesischen Kulis am
Congo und auf Fernando
Po haben dagegen sehr
schwer unter der Krankheit
zu leiden-'
Scheube (1910), p. 70.
Gor^e.
Locality
Cases
Authority
vide French Guinea
MacCarthy Island.
Locality
Cases
Authority
vide Gambia
Madagascar.
Locality
Cases
Authority
General
‘ La bilieuse h^moglobinurique
est fr<&quente dans le Nord-
Ouest de Madagascar. Sur
une population Europ^enne
tris rcstreinte nous avons eu
10 cas en deux ans et demi.*
Vivie (1903), p. 404.
* It is common in Madagascar
not only in the lower-lying
regions but also in the more
elevated district of Ant-
si anaka where it prevails
espeaally in the cool season.*
Clemow (1903), p. 47.
* 11 y a dcs nombreux cas de
fi^vres r^ittentes bilieuses,
de biUeuses h^oglobinu-
riques et d*acc^ pemideux.'
Chemin (1904).
96
Madagascar — continued.
Locality
Cases
Authority
General — {contd.)
^ £n tous les points de Tile
se rencontre I’affection ;
ndanmoins le plus grand
nombre des cas signalJs sur
les haute plateaux sont ceux
des gens qui e’^tant pro-
fond^ment impalud^s dans
les regions chaudes de la
cote montent dans les
regions froides du centre.’
65 (1897)
16 (1905)
(European troops ... 21,528)
Fontoynont (?).
Lidin(i898), pp. 490, 504, 512.
Regnier (1907).
Tananarive
Vhopital
d' I soavinandriana
‘ Pour le seul regiment d’in-
fanterie repr^sentant un
effectif moyen de 1000
hommes .... 22 dec^s par
suite d’acccs pernicieux ou
dc fievre bilieiise h^mo-
globlnurique (189K).’
Salanoiie-Ipin (191 1), p. 28.
Ankadinandriana
{native hospital)
Cases Deaths Year
I I (1904)
3 3 (1905)
23 4(?) (1906)
34 7 (1907)
‘Ce n’est qu’en 1907 gue le
diagnostic fievre btlieuse
h^moglobmurique apparait
sur ces statistiques. Nous
relevons pour cettc derniere
ann^e 41 d^c^s impu tables ^
cette affection, ce qui par
comparaison avec le chiffre
des hospitalisations et des
d^c^is hospitaliers permet-
trait de supposer environ
200 cas cn ville.’
Rigaud ( 1909).
Mananjary and Ranomajara
28 (1921-23)
Celestin (1923), p. 113.
Tananarive ...
{native hospital)
I fi 904 )
3 {^9^5)
19 (1906)
26 ^907)
Fontoynont (1908), p. 577.
Tananarive ...
41 deaths (1907)
Europeans Native Year
Troops
63 0 1897
66 2 1898
78 2 1899
109 4 1900
92 5 1901
130 25 1902
162 25 1903
Madagascar and Reunion . . .
5 deaths (1897)
Burot and Lcgrand (1897).
97
Mauritius,
Locality
Cases
Authority
General
I (1908)
‘ Je pourrais citer maints
autres excmplcs dans
lesquels la temperature a
ete heureusemcnt influencce
par la quinine.’
Scnneville (1908).
28 cases regularly treated
without quinine by Dr. de
Chazal.
Raff ray (1908).
‘ Pendant Ic cours de ma
pratique j’ai eu asoigner unc
vingtaine de cas de fievre
hemoglobinurique.’
Vinson (1908).
I (1909)
Chevreau (1909).
I (1909)
Raff ray (1909).
No records (1916-1926)
Population (1926).
Mauritius ;
(General
population 111,996
Indians ... 277,733
Chinese ... 8,507
Afauritius.
398,236
Dependencies ... 9,226
407,462
1
13(1921-1923)
Cclestin (1923), 1 14.
12 (prior to 1907)
de Chazal (1908), p. 118.
Jieau Bassin
2 (prior to 1907}
Flacq
I (1907-08)
Mesnil
I ( 1907-08)
Phoenix
8 (1907-08) !
Port Louis
3 (1907-08)
Vacao
I (1907-08)
1
98
Nossi-Bl
Locality
Cases
Authority
22
Lebeau (1851).
Le Roy de M^ricourt (1853).
Daull6 (1857).
‘ Ictero-haematuric fever, 185
cases, 49 deaths (1862-1880)’
Davidson (1892).
2
Yersin (1895).
Reunion.
Locality
Cases
Authority.
Cmrral
‘ La bilicuse h^maturique au
contmire cst moins
t'r6quente que dans Tile
voisinc (Madagascar).’
I'ontox nont (?).
1 {1873
Monestjcr (1873).
Enfin la fievrc hdmoglobinii-
rique .... n’ofFrc gen^rale-
mcnt pas ici la sev^rite qu’on
Jui r^connait a Nosi-Be.'
Mcrvellleux (1903).
St.-Denis
‘ J’ai, cn cinq ans et demi
observe, chez 45 sn'jcts 54
cas dc bilicuse h^moglo-
1 binuriquc.’
O’Zoux (191 1).
Sr. J.ouis, vide Senegal.
St. Marie.
J.ocality
Cases
Authority
*
Gouzien (191 1).
St. Thom£.
Locality
Cases 1
Authority
...
Da Costa (1906).
99
Zanzibar and Pemba Islands.
Europeans
Cases
Deaths
Native
Cases
Deaths
Year
Authority
I
0
lo
I
191^
Zanzibar Protectorate
(1916), p. 10.
-
5
'
1 9 1 L
( > 9 ^ 7 ), P- IT-
2
1 1
2
19 r7
(191 8), pp.3, 5, in.
I
n
7
I
1918
(1920). p. 1 1.
0
19^733
7
1919
0921), pp. 9, 31.
1920
t
!
1921
1
1922
J923
1924
19 LS
1926
1927
(1928), p. 9.-:.
(i) Nationality not stated.
REFERENCES
Barth £lemy-Benoit (1865). De la fievre bilicusc hematurique observee au Senegal. Arch, de
med. nav.f 4 , 4-28, 105-131, 209-225, 298-309, 379-403.
Blin (1905). Le paludisme a Mayotte. Ann. d'hyg. et de med. col., 8 , 162.
Burot, F,, and Legrand, M. A. (1897). Les troupes colonlalcs. Paris. Bailliere et fils, (not
available.)
Celestin, ly. A. -(1923). Traitement dc la fit^vre bilieuse hacmoglobinuriquc par les collobiascs
Arsenic-fer. JSull. de la Soc. Med. deVile Maurice, 38"*® Anncc, 5™® Scrie, No. 49.
DE Chazal, E. L. (1908). Observations de fi6vre bilicusp hemoglobinurique (pathogenic et traite-
ment). Bull, de la Soc. Med, de Vile Maurice, 26*"® annee, 2**'® Scrie, No. 13, i iS.
Chemin (1904). La Canonnit^rc le ‘ Capricorne ’ dans I’ocean Indien (1902-1904). Arch, dc nitul.
nav., 81 , 337-
Chevreau, P. (1909). Observation de fievre bilieuse h^moglobinuriq\ie. Bull, dc la Soc. Med. de
Vile Maurice, 27*"® Ann^e, 2“*® S6rie, No. 15, 36.
Clemow, F. G. (1903). Geography of Disease, Cambridge. 47.
Da Costa, B. F, B. (1906). Estudios sobre a ctiologia da febre biliosa hemoglobinurica. Arch.
Hyg. Path, Exot., 1 (2), 218-273. (Not available).
100
Daull£ (1857). Cinq annees d’observations m^dicales dans lea itabllssementa fran^aia de Madagascar
Cote Quest. 7 bhe inauguralc, Montpellier, Aout, 1857. (Not available).
Davidson, A. (1892). Geographical Pathology, 2 , 715- (Quotes GuUl. Arch, de med, nav. f date).
Fatome( 1907). Rapport rur Tetat sanitaire de I’Archipcl des lies du Cap-Vert. Arch, de med. nav,
87 , 246.
Fontoynont (1908). La ficvic billciise h6moglobinurlque a Tananarive, son traitement par le
\^ca-Fotsy {Aphloia theaejorniis). La Presse medicate, 16 , 577.
(1907?). Traite di hygiene. Bronardel-Chantemessc, IX. Hygiene coloniale,22j-2z%,i^^~2^%.
CouziEN (^91 1 ). Traite pratique pathologic exotique, 2 , 3 -
Lafont (1905). Geographic medicalc. Mohcli. Ann. d'lyg. et de med. col., 8 , 511-
Lafont, a. (1908). Quclques reflexions sur la fievre bilieuse hemoglobinurique. Bull, de la Soc.
Med. deVile Maurice, 26“'“ Annee, 2™® Serie, No. 14, 221.
Lf.beau (1851). These de Paris. (Not available).
Lk Roy df. MeaicouRT (1853). Th^se de Paris. (Not available).
Lidin (1898). Morbidite et mortalite a Madagascar pendant Tannee, 1897. Ann. d*hyg. et de mSd.
col., 1 , 490, 504, 512.
Mauritius, Colony of. Annual Medical Reports* for the respective Years.
Merveilleux, G. (1903). Geographic medicale. lie de la Reunion. Ann. d*hyg. et de med. col., 6 ,
225.
Monestier (1873), Fievre ictero-hematurique ou bilieuse hematurique. . Gazette des hopitaux
civils et militaires, 46 , 820.
O’Zoux, L. (1911). Cinquante-quatre cas de bilieuse hemoglobinurique a St. Denis de la Reunion.
Bull. Soc. Path. E.xot., 4 , 118.
Raffray, a. (1908). Considerations cllniques au sujet de la bilieuse hemoglobinurique. Bull, de la
Soc. Med. de Vile Maurtce, 26™® Annee, 2**^® Serie, No. 14, 225.
(*909)* Bilieuse hemoglobinurique. Bull, de la Soc. Med. de Vile Maurice, 27*"® Annee,
2“® serie, No. 15, 42.
Regnier (1907). Resume de la statistique medicale des troupes stationnees aux colonies pendant
I’annee, 1905. Ann. d'hyg. et de med. col., 10 , 396,
Rigaud, J. (1909). Traitement de la fievre bilieuse hemoglobinurique par la decoction de ‘ Voa-
Fotsy ’ {Aphloia Madagascar iensis). Ann. d'hyg. et de med. col., 12 , 389.
Salanoue-Ipin (191 1). Notes sur les causes d’insalubrite des casernements et ctablissements militaires
de Ta'hanarive. Ann. d'hyg. et de med. col., 14 , 28.
ScHEUBE, B. (1910). Die krankheiten der warmcn Lander. Vierte umgearbeitete und erweiterte
Auflage. Jena.
Senneville, E. de (1908). Action de la quinine dans la fievre bilieuse hemoglobinurique. Bull,
de la Soc. med. de Vile Maurice, 26™® Annee, 2”*® Serie, No. 14, 239.
Vay^se (1896). Un cas de fievre bilieuse hematurique observee a Mayotte. Arch, de mid. nav. et col.,
66 , * 34 -
Vinson, L. (1908). Reflexions sur la bilieuse hemoglobinurique. Bull, de la Soc. Med. de Vile Maurice,
26*"® Annee, 2”^® Serie, No. 14, 237.
ViviE (1903). Geographic medicale. Region Nord-Ouest de Madagascar. Ann. d'hyg. et de med.
col, 6 , 404.
Yersin (1895). Notes succinctes sur une epizootic des buffles, sur la typho-malarienne et la bilieuse
hematurique. Arch, de mid. nav., 64 , 49.
Zanzibar Protectorate. Annual Medical Reports* for the respective years.
ARABIA'
FRENCH WEST
AFRICA •
. ANGLO ‘EGYPTIAN
FRENCH
• • SUDAN •;
SUDAN
„,o,ER,A / J 2
iu, C0A>»T ; • •.S&^ K 4t
.ABYSSINIA
^^^^^CAMEROON^ . T. . . • • . . . . .
CONGO
i Wg .:o. B E L G I A
TANQANYIKA fe^jl-^
-^ANGOLA
^SOUTH WEST
southern ; ^
RHODESIA..
BLACKWATER
FEVER
IN AFRICA
* BECHUANALAND / §
A AFRICA
A ' TR/kNSVA;kLr >
Mm
=^AfAPE OF OOODy
BUCKM
SUSCEPTIBILITY AND RESISTANCE TO
TRYPANOSOME INFECTIONS
V. THE RESISTANCE OF RATS TO INFECTION
BY
I. J. KLIGLER
AND
R. COMAROFF
[Department of Hygiene, Hebrew Universiiy, Jerusalem)
[Received for puhlicatdon 7 February, 1929)
Host infection is conditioned on the one hand by the virus and on
the other by the host. In the common type of infection the process
may be said to consist of three phases. First there is the resistance to
invasion — the virus being either prevented from entering tlie host
or destroyed immediately on entry. As a consequence only a given
percentage of those exposed to the yirus become infected. If and
when the virus gains entry into the body of the host there follows a
period of lag or incubation, the length of which in any given host
depends largely on the dosage and virulence of the virus. Finally
there is the last and most important phase during which the host
develops ceftain specific antibodies destructive to the virus, the
final outcome depending to a large extent on the rate of evolution of
these substances by the host in relation to the rate of multiplication
and destruction of the virus.
In pathogenic protozoan infections such as malaria and trypano-
somiasis, the host-parasite antagonism differs from that observed in
bacterial infections. The first stages of the process are apparently
similar ; the last phase, however, is 'distinctly different. Even when
spontaneous recovery occurs, the immunity is a transient one and
specific antibodies are not readily demonstrable. As a rule, however,
the host ultimately succumbs after a more or less prolonged struggle.
The nature of this resistance to a protozoan infection and the various
factors influencing it has been the subject of our studies.
J03
^ 104
At present there are two views. One, supported by Taliaferro
(1922, 1926), maintains that the resistance on the part of certain
animals is essentially the same as in bacterial infections, and that
specific lytic antibodies are developed in the course of the infection.
Our own results (1924, 1926) and those recently reported by Regendanz
and Kikuth (1927), on Lewisi infections in splenectomized rats,
indicate that the resistance is essentially non-specific in character
and resides in the reticulo-endothelial system. Even the inhibitive
substance discovered by Taliaferro, in Lewisi infections, is,
according to Regendanz and Kikuth, not developed in splenec-
tomized animals.
In this connection the variable resistance of different hosts to the
same organism is of special interest. Different hosts react to
same dosage per body weight in a different manner ; the same dose
of the same strain will produce a rapidly fatal disease in the mouse,
a more prolonged infection in the rat, a relapsing type of disease in
the guinea-pig, and a chronic infection in the rabbit. The end
result is the same ; the nature and duration of the process is different.
Similarly the same dose of the same strain will cause a more rapid
evolution of the disease in infant rats than in adults and in mal-
nourished than in well-nourished animals. Variations in the dosage
of the virus also produce different results. Larger or smaller numbers
of organisms will produce a more or less rapidly fatal disease in mice
(Doerr and Berger, 1922), and rats and a shorter or longer incubation
period in guinea-pigs (Kligler and Rabinowitch, 1927).
Jt appears, therefore, that an understanding of the mechanism of
resistance can be best obtained by a combination of the two methods.
On the one hand, by observing the reactions of a given host under
different conditions, and on the other, that of different hosts under the
same conditions. In our previous contributions we followed the
reaction in the guinea-pig and rabbit under various conditions with a
view to observing the character of the resistance and, more
particularly, the nature of the relapsing infection. It was shown
that sensitising as well as immunising processes go on simultaneously,
that the resistance can be modified artificially by injuring or blocking
the reticulo-endothelial system, and that environmental and nutritive
factors played an important rdle. (Kligler and Weitzman, 1926,
Kligler and Geiger, 1928.)
105
For obvious reasons the influence of these latter factors can be
more readily followed in the rat than in the guinea-pig. In the rat
the character of the disease is simpler, the duration shorter, breeding
and nutrition more easily controlled.
As a preliminary to these studies it was necessary to elucidate the
nature and course of the infection in normal rats. In their studies on
resistance to trypanosome infections the Taliaferros (1922) concluded
that in the rat there is, as a rule, no evidence of any resistance being
built up either against the rate of reproduction or toward the destruc-
tion of the parasites. If that were the case, one would expect to
observe in the rat the same simple curve of geometric progression
noted by Doerr and Berger (1922), in mice infected with Trypanosome
gamhiense. This is not, however, the case ; neither the protocols
presented by the Taliaferros, nor the preliminary counts made by
us indicated that the progress of infection in the rat was of the
same simple character as that observed in the mouse. On the
contrary, it appeared that the rat manifested a definite resistance
probably of the destructive type, which was not observed in tlie
mouse.
Infections in mice and rats have one aspect in common. In both
animals, once the trypanosomes establish themselves in the periplieral
circulation, they increase progressively in number until the death
of the animal. In the mouse the multiplication follows a geometric
progression, the generation time remaining practically constant.
In the rat, however, the progression is irregular and the generation
time variable. These facts are illustrated by the protocols of
Doerr and Berger for mice, and the Taliaferros', and our own
observations for mice and rats. The problem to which we directed
our attention was whether the variable progression in the rat was
characteristic and, if so, what the nature of this resistance was.
Doerr and Berger (1922) assumed that the rate of multiplication
in the mouse was a function of virulence. This is probably the case
in the simple instance (the mouse) where the host is apparently
absolutely incapable of offering any resistance to the invading
parasite. In a more complex instance where the host does offer
some kiud of resistance, the rate of multiplication is a function
of host resistance as well as virus virulence. If the virulence and
dosage are kept constant, then a change in the rate of increase would
io6
indicate that resistance is offered and that there is either an inhibitive
or a destructive mechanism at work, if not both. At any rate, an
idea of the extent if not the kind of resistance offered by the rat, may
be obtained by a study of the rate of increase of various species of
trypanosomes under comparable conditions.
Methods, The course of development of trypanosomes in
infected rats was studied under conditions where other factors such
as age, dosage, etc., were kept constant. Two strains of trypano-
somes, T, evansi and T, gamhiense, were used.
The infection was followed by counts made at frequent intervals.
Early in the infection daily counts were made. As the infection
advanced, counts were made at shorter time intervals.
The rats were always inoculated with a small number of organisms
in order to obtain a true picture of the normal course of the infection.
The injection of massive doses of virus is in itself sufficient to modify
the course of the infection and lead to variable results. Blood
taken from the heart was diluted first with citrate and then with
saline, so that 0*5 or 10 c.c. contained the requisite number of
organisms. Inoculations were always made intraperitoneally.
Two counting methods were used either singly or simultaneously.
Direct counts were made in the blood counting chamber, by diluting
the blood in saline to i : 100 or i : 200 as in red cell counts. If
counts are made promptly while the trypanosomes are still alive and
sluggishly motile, no difficulty is experienced in making the count.
Usually we counted the number in 400 small squares, in order to
reduce the error. Occasionally counts were made by comparing the
number of trypanosomes with that of red cells in an ordinary blood
smear stained with Giemsa stain. Because of the progressive
anaemia in the course of the infection it is essential to make a red
cell count prior to such counts. There was always close corres-
pondence between the two methods and they could be used inter-
changeably. For counts at frequent short intervals the slide method
is preferable because slides can be prepared, labelled and counted
at leisure. , ,
Results. The results were, in the main, so uniform that it
will suffice to present a number of characteristic protocols.
107
I. Rats infected with T. evansi. (See also hg. i.)
(a) Infected with trypanosomes from guinea-pigs.
Experiment i. Rat, 98 gins, in weight, inoculated 5,000
T, evansi from guinea-pig, 19.2.28. The blood was positive on
29.2.28, after an incubation period of 10 days. Died 9.3.28.
Duration of life 19 days.
Table I.
Blood Count
Tryps. Count
Generation 'rime*
(per mm.*)
Date
Hour
R.B.C.
W.B.C.
Chamber
1 lours
2.3.28
600
4.3.28
9.00 a.m.
5,780,000
7,500
2,400
5.3.28
8.30 a.m.
200,000
1 1 1 CO t
6.3.28
8.30 a.m.
290,000
) 1 1 30
V 34
2.30 p.ni.
480,000
1 1
7.3.28
9.30 a.m.
...
660,000
) '
, 17
8.3.28
9.00 a.m.
1,960,000
‘ ]
2.00 p.m.
2,070,000
!- 00
1
9.3.28
9.00 a.m.
1,940,000
)
12.30 p.m.
1,790,000
9.3.28
p.m.
Average ...
5.3.28, a.m.,
9.3.28, a.m.
3 ^
* If we assume that the animal in question offers no resistance either of the destructive or
inhibitive type, then the increase of the trypanosomes in the circulation ought to be in the nature
of a geometric progression. In this case '
- I or - 1
Ao
where An — number of trypanosomes at the end of a given time interval Tk.
Ao = number of trypanosomes at the beginning.
r = the constant ratio, in this case 2, since the division of the trypanosomes is a simple one.
The only unknown in the equation is «, the number of intervals or divisions in time Tw.
The generation time equals the total time interval Tw, divided by the number of periods
Tn
minus one, or '
« — 1
Example ; On 6/3 8.30 a.ra. the count was 480,000 and on 8/3 9.00 a.m. 1,960,000; the
equation is, therefore, = 2 " - »
^ 480,000
or «~1 = 2.
Tw 42
The generation time =* — — — = = 21 .
« - 1 . 2
t The symbol OO is used to indicate that the apparent generation time is infinity. In reality
a microscopic examiilation of a stained specimen reveals numerous dividing forms ; what is
presumably happening is that destruction and multiplication proceed at the same rate.
io8
Experiment 1 , Experiment 2 . Experiment 3 .
Fig I
Number of Trypanosomes.
109
Experiment 2. Rat, 184 gms., inoculated 20,000 tryps.,
(T. evansi from guinea-pig) on 17.4.28. Blood positive, 22.4.28.
Duration of life 16^ days.
Table II.
Blood Count
Tryps. Count (icneration Time
R.B.C.
Chamber Days
16.4.28
6, 1 60,000
22.4.28
occ.
23.4.28
2,000 ]
' 00
24.4.28
9.45 a.m.
4,880,000
2,000 )
25.4.28
9. 15 a.m.
Ncg.
12.15 p.m.
...
2,000
26.4.28
10.00 a.m.
2,000 )
Hi
27.4.28
1. 10 p.m.
8,000 1 1
29.4.28
10.00 a.m.
1
46,000 L 21
30.4.28
10.00 a.m.
5,020,000
j ' 60,000 )
1.5.28
3.45 p.m.
4, 590,000
j 698,000 j
5.00 p.m.
^ !8
1
==• 5=8
9.45 a.m.
5,050,000
1,180,000 ^
12.00 noon
4,360,000
1,150,000
00
3 20 p.m.
4,340,000
1,230,000 j
3 - 5-=8
8.40 a.m.
3,360,000
1,166,000 /
11.55 a.m.
1 , 1 90,000
4.00 p.m.
3,000,000
1,024,000
Heart
4.55 p.m.
2,350,000
1,300,000
3.5.28
4.55 p.m.
...
no
(ft) Infected with trypanosomes from rat ; first passage from
guinea pig.
Experiment 3. Rat, 88 gms., weight inoculated 5,000 tryps.
from rat, first passage. Incubation 10 days. Duration of life
20 days.
Table III.
Date
Time
Tryp. Count
Generation Time
Hours
29.2.28
+
1.3.28
+
2.3.28
4 -
4 - 3-28
+
5 - 3 .J 8
2.00 p.m. 1
50,000
)
16
6.3.28
9.15 a.m.
1 50,000
)
6.3.28
2.45 p.m.
290,000
21
7.3.28
9.00 a.m.
520,000
)
1 00
8.3.28
9.00 a.m.
680,000
1 J
24
9.3.28
9.30 a.m.
1,540,000
]
*
1. 00 p.m.
1,480,000
h 00
10.3.28
9.00 a.m.
1,810,000
) •
I i.oo a.m.
1 ,680,000
-f == Trypanosomes present in stained drop but too small in number to count.
Ill
(c) Infected with trypanosomes from rat ; 3rd passage.
Experiment 4. Rat, 232 gms., inoculated 6,000 tryps. {T.
evansi, 3rd rat passage) on 25.3.28. Blood positive 7.4.28. Incuba-
tion 13 days. Duration of life 18 days.
Table IV.
Date
Hour
Blood Count
Tryps.
Count
Generation Time
R.B.C.
Chamber
Smear
Hours
26.3.28
7,870,000
7.4.28
a.ra.
7,480,000
28,000
-
00
8.4*28
1 1. 00 a.m.
5,950,000
34,000
1
9.4.28
1 1. 00 a.m.
138,000
4.45 p.m.
318,000
10.4.28
9.00 a.m.
410,000
2.45 p.m.
3,840,000
556,000
■
24
11.4.28
9.30 a.m.
3,910,000
950,000
2.00 p.m.
930,000
••
48
12.4.28
8.30 a.m.
4,100,000
1,254,000
1,391,600
2.40 p.m.
1,200,000
3.40 p.m.
2,680,000
i
_
T, 1 88,000
112
(i) Infected with trypanosomes from rat ; 4th passage.
Experiment 5. Rat, 84 gms. in weight, inoculated 15,000 tr5^s.
from rat, 4th passage. Incubation 10 days. Duration of life 22 days.
Table V.
Date
Count?
Generation Time
R.R.C.
Trvps.
Hours
26.4.28
...
5,740,000
Occasional
6.5.28
...
...
8.5,28
9.00 a m.
5,480.000
Negative
9.5.28
9.00 a.m.
...
Negative
10.5.28
10.00 a.m.
5,000,000
4,000
1
11.5.28
10.00 a.m.
6,000
! -8
)
13.5.28
10.00 a.m.
3,980,000
12,000
)
14.5.28 '
1. 00 p.m.
28,000
24
1
1
1
6.00 p.m, j
4,230,000
58,000
! 18
15.5.28 1
12,00 noon
j
4,100,000
76,000
J
i
6.00 p.m.
...
146,000
- 10
16.5.28
10.00 a.m.
4,200,000
284,000
17.5.28
9.00 a.m.
4,230,000
588,000
1
5.00 p.m.
0
00
780,000
!
18.5.28
9.00 a.m.
3,700,000
1,150,000
)
12.00 noon
3,440,000
1,200,000
1. 15 p.m.
2,040,000
•
...
“3
II. Rats infected with T. gamhiense. (See also fig. 2.)'
(a) Infected with T. gambiense from rat ; 2nd passage.
Experiment 6. Rat, 59 gms., inoculated 20,000 trypanosomes
from rat, 2nd passage Incubation period 6 days. Duration of life
19 days.
Table VI.
t)ate
Hour
Count
Generation Time
Red Cell
Tryps.
Hours
26.3.28
9.00 a.m.
7,960,000
2,000
9 a.m., 26-27 --- 12
5.00 p.m.
4,000
27.3.28
9.00 a.m.
X,ooo
.
5.00 p.m.
1 6,000
9 a.m., 27 2S 16
28.3.28
9.00 a.m.
22,000
3.30 p.m.
42,000
9 a.m., 28-3 p.m., 29 = 15
29.3.28
9.00 a.m.
68,000
3 p.m., 28-3 p.m., 29 = 24
12.00 noon
80,000
9 a.m., 29-30 = 24
3.30 p.m.
4,360,000
86,000
30.3.28
9.00 a.m.
3,240,000
108,000
9 a.m., 30-31 =
1 1. 00 a.m.
130,000
2.00 p.m.
96,000
9 a.m., 31-1 12
3-30 p-m.
122,000
31 - 3-28
9.00 a.m.
1 56,000
12.00 noon
156,000
9 a.m., 1-2 — 24
1.4.28
9.00 a.m.
602,000
3.30 p.m.
712,000
2.4.28
8.30 a.m.
2,600,000
1,084,000
9.15 a.m.
...
i, 33 S>ooo
"4
28.3 29.8 SO.S 31.3 l.i 2.4 7.4 8.4 9.4 10.4 11.4 19.4 10.5 11.5 12.5 13.5
Experiment 6. Experiment 7. Rat A.
Note the contrast in the character of the first two curves as compared with
the last which approximates that of the mouse.
Fig 2.
Number of Trypanosomes.
IIS
{b) Infected with T. gambiense from rat ; 3rd passage.
Experiment 7. Rat, 74 gms. in weight, inoculated 6,000
r. gambiense from rat, 3rd passage. Incubation 9 days. Duration of
life 18 days.
Table VII.
Date
Hours
Count
Generation Time.
R.B.C.
Chamber
Smear
Hours
7.4.28
8.4.28
a.m.
6 , 68 ojOoo
34,000
...
GO
p.m.
...
30,000
24
9.4.28
9.00 a.m.
...
70,000
12
10.4.28
' 10.00 a.m.
256,000
24
10.4.28
3.00 p.m.
...
408,000
11.4.28
II. 15 a.m.
3,360,000
600,000
24
12.4.28
11.15 a.m.
3,370,000
1,100,000
1,196,350
1 2.15 p.m.
1,313,000
1
j
1
[ 4.00 p.m.
5,30 p.m.
...
1,356,000
1,390,000
(Heart blood)
Experiment 8. Rat, 72 gms., inoculated 6,000 T. gambiense
from rat, 3rd passage. Incubation 8 days. Duration of life 17 days.
Table VIII.
Date
Hour
Count
Generation Time
R.B.C.
Tryps.
Hours
4.4.28
6.4.28
7.4.28
a.m.
a.m.
9.00 a.m.
6, 1 50,000
20,000
350.000
728.000
12
24
8.4.28
9.00 a.m.
5,680,000
660,000
00
1.00 p.m.
4.00 p.m.
600.000
700.000
CO
9.4.28
10.00 a.m.
600,000
1. 00 p.m.
3 30 P-m.
2,780,000
458.000
478.000
24
10.4.28
9.00 a.m.
***
1,300,000
12.00 noon
778,000
1.00 p.m.
776,000
oc
2.30 p.m.
2,800,000
684,000
11.4.28
8.00 a.m.
.. . .1
1,620,000
(Heart blood)
Discussion. It is apparent from the protocols and curves
presented above that the infectious process in trypanosome infected
rats is not a simple one. Before the organisms have definitely
invaded the circulation, as well as after they have established them-
selves, there are fluctuations in the numbers of trypanosomes and
the growth curve is quite different from that observed in mice.
An analysis of the protocols presented by the Taliaferros shows that
their results correspond with ours. Rats 709 and 729 show a definite
relapsing type of infection, while Rats 703 and 705 manifest the same
general irregularity in the generation time as do our rats. Another
point of interest is that the same strain in mice not only shows a
smooth growth curve, but a much lower average generation time
than it does in rats. In the mouse infected by them with
r. rhodesiense, for example, the generation time fluctuates around
6 hours and the average is 6 5 hours, whereas in the rats presumably
infected with the same strain, the generation time varies from 6 hours
to 48 hours, and the average is 17 to 18 hours (Rats 703 and 705).
These irregularities can only be accounted for by assuming that
the rat possesses some mechanism of resistance which does not
exist in the mouse. This mechanism is probably similar in kind to
that present in the guinea-pig, although different in degree. Experi-
ments not yet completed indicate that the injection of olive oil has a
similar depressing effect on the resistance of rats as it has on guinea-
pigs. In the latter the Taliaferros postulate a destructive type of
resistance because the coefficient of variation of the developing
trypanosomes which is a measure of rate of growth is constant.
That this is also the case in our rats is indicated by the fact that there
is an active state of division as well as an actual rise and fall in the
numbers of trypanosomes at all stages of the infection. If this
assumption is accepted as valid, and the rate of multiplication is
constant, then it follows that the variations in the generation time
in infected rats at different stages of the process is due to a variation
in the rate of destruction. This destructive process must go on in
the rat throughout the entire period of infection, even in the early
stages before the hypothetical antibodies have had time to develop,
since variations in numbers are just as common in the early as in the
late stages of the infection.
These experiments do not solve the problem as to the nature of
the mechanism responsible for the destruction. Large amounts of
serum taken from a rat at the height of the infection, and injected
into another infected rat, produces no effect on the numbers of
trypanosomes or on the course of the infection. At the same time,
it is possible occasionally to obtain an infection in a treated rat which
corresponds closely with that observed in mice. In one experiment
a group of rats were infected with T. gambiense. The infection
failed to develop, presumably because the dilution process left a
smaller number of organisms in the inoculum than was expected.
Three weeks later these rats were re-infected with 25,000 organisms
of the same strain. All the rats of the series showed a lower incuba-
tion period (4-5 instead of 8 days) and shorter duration of illness
(10 J instead of 18 days), and some of them showed growth curves
ii8
approximating that in mice (see fig. 2). The protocols of two of these
rats is presented below. The others were less regular but of the
same general character.
Table IX.
i
A
Generation Time
B
66
Generation Time
Weight
244
Count
Hours
Count
Hours
Infected 12.4.28
Re-infected, 4.5.28
...
8.5.28, 8.20 a.m.
9.5.28,
10.5.28, a.m.
11.5.28, a.m.
20,000
128,000
8
44,000
12.5.28, a.m.
I3'S-28, 9.50 a.m.
1,032,000
16
708,000
12
11.30 a.m.
1,320,000
...
6*
5.00 p.m.
...
...
1
1,401,000
)
Average 12
Average 1 1
Similar effects may be obtained by an injection of oil prior to an
infection. In other words, rats treated so as to induce a depression
of the resistance mechanism develop an infection which approximates
that observed in the mouse. It would seem from these observations
that we are dealing with a resistance mechanism which varies in
degree in these different animals, being practically nil in the mouse,
moderate in the rat and much more highly developed in the guinea-
Pig-
The cause of death in trypanosome infections is a question of
considerable interest. Doerr and Berger called attention to the fact
that in their mice death occurred when the number of trypanosomes
reached a certain fairly constant concentration per cubic millimeter
of blood. We observed a similar relation in our rats. The average
number of trypanosomes per cubic millimeter at or shortly before
exitus was 1,440,000 in ii rats infected with T. evansi, and 1,420,000
in 14 rats infected with T. gamhiense. It is not certain, however.
whether the number has a direct causal relation to the death and
the shock which precedes it or whether the number is incidental to
other concomitant factors which are responsible for death, the latter
limiting the number of trypanosomes per unit volume. In this
connection it is of interest that different species of trypanosomes
apparently reach a different limiting concentration. From the
protocols presented by the Taliaferros it appears that in infections
with r. rhodesiense death ensues when the number per cubic
millimeter is about 3,000,000. In T. equiperdum the number
reaches 5,000,000 and in T. equinum 10,000,000. In our experiments
with infant rats (11-12 gms.) death occurred when the number
was only 750,000. It is noteworthy that in all cases the red cell
count at time of death was greatly reduced, often to about 2,500,000,
or about one-third of the original count. In experiments now in
progress we have noted a constant increase in the lactic acid
concentration of the blood parallel with the increase in the number of
trypanosomes. These experiments will be reported in another
communication.
Whatever the immediate cause of death may be, there is a direct
connexion between it and the number of organisms in the blood
stream. The difference in the final concentration of trypanosomes in
infections with different species might be due to a difference in the rate
of fermentation, so that the ultimate injury resulting in death is
produced only by a larger number of organisms. If this proves to be
the case, we have both a simple explanation of their pathogenicity,
as well as a method for differentiating some of the species of
trypanosomes.
SUMMARY
A study was made of the course of a trypanosome infection in rats
and of the character of their resistance to such infections. The
investigation was carried out by following the course of infection in
rats by repeated counts of the nfimber of trypanosomes in the
circulation. An analysis of the data indicates that : —
I, The infection in the rat is of an order intermediate between
that in the mouse and guinea-pig. The rat possesses a resistance
which is probably the same in kind as, but different in degree from
that of the guinea-pig.
120
2. Although the infection is a progressive one there is a constant
destruction of trypanosomes throughout the course of infection.
3. Depression of the resistance may result in an infection which
approximates more closely that of the mouse. This phase of the
question is now under investigation.
4. At time of death the concentration of trypanosomes in the
circulation is constant. For the species studied, the average numbers
were 1,440,000 for T. evansi, and 1,420,000 for T. gamhiense.
The red cell count is also greatly reduced, but varies a great deal
more than the trypanosome count.
The direct causal relation of these factors to death of the animals
is not certain. It appears, however, that death is due to injury
produced by the metabolic products of the trypanosomes (lactic acid)
and that the organisms must reach a certain concentration, which
differs with different species, before they can affect the changes or
intoxication which lead to death. Disturbance in the oxidation
mechanism is probably a critical element in the process.
REFERENCES
Doerr, R., and Berger, W. (1922). Beziehungen zwischen Virulenz und Vermchrungsgcsch-
windigkeit dtr Erreger. Ztscbr. fiir Hyg, und Infekt., 95, 319.
Kligler, I. J., and Geiger, A. (1928). Relation of salt deficient diet to infection. Proc, Soc. Exp.
Biol. Med., 25 , 385.
(1928). Lactic acid production in trypanosome infected rats. Proc. Soc. Exp.
Biol. & Med. (in Press).
and Rabinowitck, G. (1927)- Susceptibility and resistance to trypanosome infections.
, III : Relation of dosage to course of infection. Ann. *Irop. Med. ^ Parasitol., 21 , 375*
and Weitzman, Iw (1924). Experimental study of trypanosomiasis. Ann, 7rop.
Med. & Parasitol., 437-
(1926). The nature of immunity to a protozoan infection. Proc. Soc. Exp.
Biol. dEf Med., 23 , 355.
(1926). Susceptibility and resistance to trypanosome infections. II ; The relation
of physical environment to host susceptibility to infection, Jl. Exp. Med., 44 , 409.
PzARCC, L., and Brown, W. H. (1918). Experimental trypanosomiasis : its application to
chemotherapeutic investigations. Jl. Exp. Med., 28 , 109.
Regendanz, P., and Kikuth, W (1927). Uber die Bedeutung der Milz fiir die Bildung des
Vermehrungehinderenden Reaktionsproduktes (Taliaferro) und dessen Wirkung auf den
Infektionverlauf der Ratten Trypanosomiasis (T. lezoisi). Cent./, Bakt. Orig.^ 103 , zji.
Taliaferro, W. H., and L. G. (1922). The resistance of different hosts to eEperimental tryapnosome
infections with special reference to a new method of measuring this reristance. Amer. Jl.
264.
and Johnson, T. L. (1926). Zone phenomena in in vivo trypanolysis and the
therapeutic value of trypanolytic sera. Jl. Prev. Med., 1 , 85.
THE EARLY LIFE HISTORY OF
CREPIDOBO THRIUM TESTUDO
(Magath 1924)*
BY
THOMAS B. MAGATH
(Section on Clinical Pathology, The Mayo Clinic,
Rochester, Minnesota)
(Received for publication 14 February, 1929)
Plate III
In 1924 I described a cestode as Ophiotaenia testudo, from the
soft-shelled turtle (Antyda spinifera). Nybelin's (1917) paper on
Australian cestodes, which were collected during Dr. Mjoberg’s
Swedish Scientific Expedition to Australia, was not available to me
and I did not know that he considered the genera Ophiotaenia,
Ophidotaenia and probably Solenotaenia as synon5mous with
Crepidobothrium. Although it is not necessary in this paper to
consider his arguments for such synonymy in regard to Ophiodotaenia
and Solenotaenia, it is desirable to point out that he considered
La Rue’s genus Ophiotaenia not to possess sufficient distinguishing
characters to separate it from the earlier named genus.
La Rue, in discussing the validity of Ophiotaenia, stated that
* while in the structure of the proglottids and in the arrangement of
the genital organs this species (C. gerrardii) agrees almost perfectly
with the Ophiotaenia, there remain two characters which are deemed
of sufficient value to warrant a separation of the snake Proteo-
cephalids into two genera. These characters are the structures of
the suckers and the length of the neck.’
Nybelin found in certain individuals of C. mjObergi that some of
the suckers were re-entrant and some were not, thereby negativing
one of the two characters pointed out by La Rue. The other
character, the length of the neck, does not appear to be of sufficient
importance to justify the separation of the genera. The most
that could be said concerning the length of the neck would be that
it might play a part in the separation of species but when one realises
the great variation in the length of various organs and parts in an
• Read before the American Society of Pararitologists, New York City, December 27 to 29, 1928.
I2I
122
individual species, it is evident that the length of so elastic a structure
as the neck is not of generic importance. Furthermore, in the generic
characterisation of Ophiotaenia, La Rue does not mention the neck.
There being no other distinguishing characteristics in the genus as
opposed to the genus Crepidobothrium it appears that Nybelin's
contention is valid.
Meggitt (1927), in discussing the validity of certain genera
belonging to this group of worms, agrees with Nybelin and with
him places the^ three genera in question as synon5mious with
Crepidobothrium. He accepts the genus Ichthyotaenia Lonnberg
(1894), in preference to Proteocephalus Weinland (1858). The only
other three genera in the family which he accepts are
Corallohothi^ium Fritsch (1886), Gangesia Woodland (1925), and
Crepidobothrium Monticelli (1899) ; the latter, in addition to the
three genera already mentioned should according to Meggitt
contain Acanthotaenia shipleyi Linstow (1903). As synonyms of
Ichthyotaenia, he gives Acanthotaenia Linstow (1903), Bactrachotaenia
Rudin (1917), and Choanoscolex La Rue (1909).
It is unfortunate that Meggitt’s (1927) article has suffered from
what is evidently poor proof-reading for it often leaves one somewhat
in doubt as to the author's meaning. Besides the fact that he has
given as many as three different dates for the naming of a genus
and two different spellings for the name of a species and has stated
that the only Corallobothrium species is lobosum Riggenbach (1895),
a similar error being made by Woodland (1925), there are certain
other more serious errors in the text. He states that in C. testudo
(Magath, 1924) there are from fifteen to twenty uterine pouches,
whereas the original description states that the number of pouches
is from fifteen to twenty-five. After arguing, on page 81, that the
species testudo should be placed in the genus Crepidobothrium, he
places it in the genus Ichthyotaenia on a subsequent page. This is
evidently a curious error because in the key of species of the latter
genus he lists I. magna (Magath, 1924) ; then in the table of species
he lists the species as I. testudo (Magath, 1924). Evidently it should
be the species of Hannum (1925). On page 77 he states that
C. gerrardii (mis-spelled gerrardi) and C. paraguayensis appear to be
identical in spite of the fact that C. geftardii and C. perspicua are the
only two members of the group given in his table ' D ' that possess
an apical organ and the genital pore in C. paraguayensis is anterior
and in C. gerrardii is central. In short, there is as much difference
as given in his own table between these two species as any other two.
He further says that the species * magna, monnigi, schultzei [mis-
spelled schuUzt]^ testudo and hylae are stated to have the testes in two
fields, but with the vagina anterior or posterior ; no statement is made
whether the vagina is invariably constant in position ; only in
filaroides is this the case.' In the description of C. testudo, I stated
on page 46, ' The vagina always lies anterior to the cirrus pouch.*
Finally, one should point out the fact that his descriptions of the
new species do not differ in general from those of previous authors.
Sandground (1928) described two new species of cestodes and
re-described a third, all of which he placed in the genus Ophiotaenia,
He did not discuss the validity of the name except to show that he
was cognizant of the work by Nybelin, Woodland and Meggitt, but
he did point out that Fuhrmann (1924) still retains La Rue's genus.
However, on examination of Fuhrmann’s paper one finds that
while it contains a description of a species there is no discussion of
the validity of the genus Ophiotaenia. Furhmann did not refer
to Nybelin's work which might be taken to indicate that he had not
examined it.
While it does not seem wise at this time to accept Woodland's
(1925) sweeping revision of the Proteocephalids, although there is
argument in favour of it, it seems to me clear that Ophiotaenia is
synonymous with Crepidohothrium.
Being impressed by the fact that the only identifiable food in the
stomach of more than one hundred soft-shelled turtles examined
were crayfish, and that no crayfish had been seen in the more than
two hundred hard-shelled turtles examined, together with the fact
that C. testudo was never encountered in hard-shelled turtles and was
present in soft-shelled turtles, I suggested that the life-history of the
worm might have something to do with crayfish. Further work on
this line had demonstrated that the crayfish probably does not enter
into the life-history of the species. "
Profiting by the excellent work done on the early life-history
of certain cestodes by Essex (1927, 1928), I have investigated the
life-history of C. testudo and am now able to describe the first stages.
For the history of the subject and general procedure the reader is
referred to the papers by Essex.
Eggs may be obtained in large numbers by placing pieces of the
124
adult worm in tap water, and masses of eggs may be seen to be
extruded all along the worm. The description of the eggs which
was given earlier (1924) was made from preserved material, hence the
following description made from living material is more accurate.
The size of the outer membrane varies a great deal, but in mature eggs
(Plate III, fig. a) it ranges from 6ofi to loofi in diameter. This
membrane is thin and transparent, containing thin mucoid fluid which
contains the oncosphere surrounded by another covering. This
covering consists of a membrane beneath which is a layer of granular
material in which one sees globules of some more refractive material.
This covering is about 10 fx thick and inside it is the oncosphere. So
far as I am able to see, there is no third membrane between the second
membrahe and the oncosphere.. In this I agree with Essex (1928)
and further consider the second covering homologous to the shell
of such eggs as T. saginaia. There is certainly no jdelimiting inner
membrane to the granular second covering for if it is ruptured the
contents flow out, leaving only the thin outer membrane of the
second covering, and although I tried repeatedly, it was never
possible to demonstrate a third covering.
The six-hooked oncosphere has an average diameter of 20;w and,
with the second covering, is 40/^ in diameter.
The mature embryo is motile within the second membrane but
seems unable to free itself from the shell. The six booklets invariably
have the blade of the booklet toward the centre of the oncosphere
and the booklets are in pairs. They are about 5^ long and the
hook itself appears to be little more than a slight projection from,
or knob on, the shank.
^Following the usual procedure, a large quantity of eggs was
placed in an aquarium with various samples of plankton. This
particular material contained at least three unidentified species of
Cladosera, one species of Diaptomus and Cyclops leuckarti and Cyclops
bicuspidatus. During the course of the experiments two hundred
Cladoserae and twenty Diaptomi were examined, but none was found
to contain the larval forms of C. testudo. The two species of Cyclops
ate the eggs of the tapeworm readily in the manner described by
Essex (1928). However, no development took place in
C. bicuspidatus. In one experiment, after feeding C. bicuspidatus
with eggs, seven were examined 72 hours later, six after 96 hours,
twelve after no hours, and five after 132 hours, with negative results.
On the other hand, every C. leuckarti examined (eighty- two in all)
after it had been in contact with these eggs, contained the developing
oncosphere in numbers from one to twelve. In view of this, together
with the fact that the development of the oncosphere was progressive
with time, supports the conclusion that C. leuckarti is a natural first
intermediate host for C. testudo.
As soon as the oncosphere reaches the body cavity of the Cyclops,
which takes place in at least six hours, it has become quite active,
extending and contracting, but for the most part retaining a spherical
shape. The booklets, now fully formed and about lo^ long
(Plate III, fig. d)y can be thrust out from the limiting membrane and
now it is observed that the larvae seem to move with the booklets at
the anterior end, but the hook part of the booklet is now near the
periphery of the animal, opposite its position when the oncosphere
was enclosed in its shell. This fact I have never seen referred to and
since the booklets have never been seen to turn over, it must be
concluded that they immediately begin to pass backward through the
body of the oncosphere. Essex (1928) illustrated the same thing in
his drawing, but did not comment on it. Hunter (1928) has
represented the booklets in the same relative position in the egg
(opposite to the way I found them) as in the early larva.
The motion of the booklets is interesting. As the larva contracts
they appear with the two lateral pairs horizontal and in the same
straight line, with the central pair at right-angles. When the larva
elongates, the three pairs become parallel. This alternating contrac-
tion and extension is often quite rapid.
Variation in size in the growing larvae is great and depends
somewhat on the number the Cyclops ingests, hence the figures given
will be for typical oncospheres at different stages. They were
studied alive in 0 5 per cent, solution of sodium chloride because
plasmolysis took place in water. Plate III, fig. 6, illustrates an
oncosphere which had been fed 47 hours earlier and it was 40^ in
diameter. After another forty-eight hours a Cyclops was examined
which harboured ten oncospheres, the largest being 60 /jl in diameter
(Plate III, fig. c), and still spherical. After that, the larvae elongate
and the booklets remain posterior. After another twenty-four hours
the largest larvae appear as in Plate III, fig. c, and have an average
length of from 0160 mm. and 0 090 mm. wide. They are capable of
a great deal of extension and begin to assume more of a ribbon shape.
126
Hooklets are often left in the body of larvae and after another forty-
eight hours have elapsed the end away from the hooklets is definitely
established as the head end. However, the larvae have practically
reversed their polarity after the ninety-six hour stage. The form is
capable of constricting at irregular intervals so that the hooklets
eventually are contained in a small rounded ball at the posterior end
and the head end is often pushed out in a knob-like form. This does
not become permanent until the next day when the so-called end
organ appears as an urn-like structure with an anterior indentation.
Eight days after the Cyclops has been fed, the end organ is fully
formed and is 50// in diameter. It can be protruded and retracted.
At this time the cercomer is formed, containing the hooklets, and is
25// long. On the seventh day calcareous bodies appear and are
arranged in two lateral rows (Plate III, fig./), about eight in each row.
The larvae are very active, moving constantly in the body of the
Cyclops. They constrict themselves at different places and elongate,
changing into grotesque shapes.
The next stage in their development takes place during the next
twenty-four to forty-eight hours, when the four suckers make their
appearance (Plate III, fig. g). They are especially noticeable when
the larvae are elongated and appear as crescentic thickenings 38//
long. Although the embryos assume various shapes there is a
definite tendency to constriction in a region which may be termed the
neck. This accentuates the head and the body assumes an elongated
appearance. There is further development of the end organ and
suckers during the next few days, and the calcareous bodies become
irregularly scattered throughout the body, but there is none in the
head.
When the larva is twelve to thirteen days old its motility becomes
less and it begins to contract more and more until finally the head
invaginates into the body and the larva assumes the shape of a
pear (Plate III, fig. h). The head often rotates (Plate III, fig. i ) so
that as one looks at the larva from the side, the end of the head
presents itself. In this position the end organ and suckers are clearly
defined. The larvae average 0180 mm. long and 0120 mm. broad at
the greatest diameter. The end organ is 50// in diameter and the
suckers 38// in diameter. After fourteen days the larvae cease to
undergo further development except that the cercomer drops off.
127
The larvae are incapable of locomotion, but a churning movement
of the protoplasm and the head is seen.
The part of the life-history between this phase and the appearance
of the worm in the intestine of the turtle must for the present remain
a matter of speculation, as must the nature and disappearance of the
end organ. I have seen larval cestodes in the livers of fishes, which
have heads suggesting the genus Crepidohothrium but possessing end
organs. It may be that the infested Cyclops, when eaten by fishes,
are freed of their parasites and that the worms find their way to the
liver, there to encyst and be eaten in turn by turtles. I have been
unable to ascertain whether soft-shelled turtles eat fish and I have
never seen one in their stomachs, but they are swift enough to catch
them and they may even obtain the plerocercoids from dead fish,
or, of course, they may obtain the worm directly from the Cyclops.
The large numbers of tapeworms seen in turtles and the failure to
observe very small worms in the intestine rather argues against the
last method of infestation. This subject will be studied later.
SUMMARY
The author agrees with Nybelin that the genus Ophiotaenia is
synonymous with Crepidohothrium.
The early life-history of C. testudo (Magath, 1924) is described.
It takes place in Cyclops leuckarti in fourteen days.
REFERENCES
Essex, H. E. (1927). Early development of Diphyllobothrium latum in Northern Minnesota.
Jl. Parasitol.f 14, 106-109.
(1928). The structure and development of Corallobothrhm. Illinois Biol. Monog., 11.
Fuhkmann, O. (1924). Two new species of reptilian cestodes. j4ftn. Trop. Med. Parasitol.^ 18,
5°5-5n-
Hunter, G. W. (1928). Ill : Contributions to the life history of Proteoccphalus ambloplitis (Lcidy).
yi. Parasitol., 14, 229-242.
La Rue, G. R. (1914). A revision of the cestode family Proteocephalidae. Illinois Biol. Monog.., 1.
Magath, T. B. (1924). Ophiotaenia testudo^ a new species from Amyda pinifera. Jl. Parasitol.j 2,
44-49.
Meggitt, F. J. (1927). Remarks on the cestode families Monticellidae and Ichthyotaeniidae. Ann.
Trop. Med. ^ Parasitol., 21, 69-87,
Nybelin, O. (1917). Results of Dr. E. Mjoberg’s Swedish Scientific Expedition to Australia, 1910-
1913, XIV. Australiscbe Cestoden-Kundl. Svenska Veten. Handl.y 52, i“48-
Sandground, J. H. (1928). Some new cestode and nematode parasites from Tanganyika Territory.
Proc. Boston Soc. Natural History y 39, 13 1- 150.
Woodland, W. N. F. (1925). On three new Proteocephalids (Cestoda) and a revision of the genera
of the family. Parasitol.y 17, 370-394.
128
EXPLANATION OF PLATE III
Fig. a. Mature ovum of C. testudo.
Fig. b. Embryo from C. leuckarii.
Fig. c. Embryo from C. leuckarii.
Fig. Hooklet from embryo.
Fig. e. Embryo from C. leuckarii.
Fig. /. Embryo from C. leuckarii showing cercomer and end organ.
Fig. g. Head of embryo from C. leuckarii showing end organ and
suckers.
Fig. h. Embryo from C. leuckarii after head has invaginated.
Fig. i. Embryo from C. leuckarii after cercomer has dropped off.
MISCELLANEA
STRONGYLOIDOSIS OF THE WOOLLY
MONKEY (LAGOTHRIX HUMBOLDTIJ
{Received for piMication, 13 February, 1929)
In November, 1928, one of us (A. W. N. P.) received the stomach
and intestines of a Central American monkey, which had died after
showing marked vomiting, diarrhoea, and great loss of flesh. After
some correspondence we think it was shown that the species in
question was Humboldt’s Nigger Monkey, or Woolly Monkey
{Lagothrix humholdti). This species is ofteft kept as a pet in this
country.
On the outside of the small bowel, a male and female Dipetalonema
gracile were found.
These long, and slender filariid nematodes live within serous
cavities, and rarely produce disease.
The faeces contained numerous Strongyloides eggs, and scrapings
from the mucous membrane showed large numbers of parasitic
females of this genus. The following average measurements were
obtained from five specimens : length, 4 86 mm. ; length of
oesophagus, -86 mm. ; vulva to tip of tail, 1-94 mm. ; anus to tip
of tail, 8i/r. The vulva and anus were salient, and the striations
were well marked. It is, therefore, suggested that the species is
5 . papillosus in the widest sense, and in accordance with the views
expressed by Chandler (1925).
A damaged ancylostome was also found, which proved to be
A ncylostoma duodenale.
Although there is some dispute as to the pathogenic effects of the
different species of Strongyloides, it would appear from the history,
the clinical account of the case, and the details of the post-mortem
examination furnished by the sender, that the monkey’s illness and
death were due to intestinal toxaemia resulting from Strongyloides
infestation. A point of additional interest is the presence of the
human ancylostome in an animal which enjoyed the company of man,
A. W. N. Fillers.
T. Southwell.
REFERENCE
Chandler, A. C. (1925-) The species of Strongyloides (Nernatoda). Parasitology, 17 , 426.
12Q
A NOTE ON A NYMPHAL LINGUATULID—
LEIPERIA CINCINALIS Sambon— FROM THE
MUSCULATURE OF THE FISH TILAPIA
NILOTICA
{Received for publication, 13 February, 1929)
In July, 1928, Mr. S. C. J. Bennett, M.R.C.V.S., of Khartoum,
forwarded to one of us (A. W. N. P.), a pentastome which he had
collected from a cyst in the flesh of a river fish known on the Upper
Nile as bulti {Tilapia nilotica). The preservative was apparently
alcohol of unknown strength.
The specimen was a- nymph measuring about 3-5 cms. in length,
by 2 mm. in diameter at the thicker anterior end, and i mm. at the
narrower posterior extremity. It was cylindrical, and slightly
flattened in front. The colour was reddish-yellow. Throughout its
length the cuticle was annulated, there being about no equi-
distant grooves.
The anterior extremity was rounded, and slightly bent towards
the ventral aspect. Just behind the anterior border there were
four openings, the two foremost of which werp close together,
whilst the posterior pair were more widely separated. From each
of these openings there protruded a yellowish coloured, smooth,
common trunk, which branched into two curved and sharply-pointed
hooks. The anterior branch in each case was smaller and less
curved than the hinder one. The smaller (anterior) measured
about 2io/« in length, and the larger about 250^.
According to Diesing, the mouth is between the origins of the two
hinder double hooks.
No further details of the structure could be made out. Taking
into consideration the host, and the locality from which it was
ccdlected, it appears that the nymph can be placed in the ' group '
Pentastomum gracilis. This name, according to Sambon (1922),
has been applied to a number of immature linguatulids belonging
to the genera Sebekia and Leiperia, of the Sebekini division of the
sub-family Porocephalinae.
The hooks in the present* specimen were very similar to those
figured by Sambon for the adult Leiperia cincihalis from the Nile
crocodile, and it is therefore considered that the nymph belongs to
this species.
T. Southwell.
A. W. N. PiLLERS.
REFERENCE
Sambon, L. W. (1922.) A synopiis of the family Linguatulidat. Jh ^ 85 , 188,
jU
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Volume XXIII
June 27, 1929
No. 2
ANNALS
OF
TROPICAL MEDICINE AND
PARASITOLOGY
issui;i) RY
THE LIVERPOOL SCHOOL OE TROPICAL MEDICINE
Edited by
PRortssoR WARRINGTON YORKE, M.D., M.R.C.P.
PkoFiissoR D. B. BLACKLOCK, M.D.
Professor W. S. PAITON, M.B,
Emeritus Professor R. NEWSTEAD, E.R.S.
THE INCORPORATED
LIVERPOOL SCHOOL OF TROPICAL MEDICINE
Founded by Sir ALFRED LEWIS JONES, K.C.M.G
{Affiliated xmih the University of Liverpool)
Hon. President : H.R.H. The Duke of York, K.G., G.C.V.O.
Chairman : Sir F. C. Bowring.
Vice-Chairman : Professor E. W. Hope, O.B.E., D.Sc., M.D.
Hon. Vice-Presidents : The Earl of Derby, K.G., G.C.V.O., C.B., LL.D
Baron Kylsant, G.C.M.G.
Sir Edward Merewether, K.C.V.O.
Sir H. J. Read, K.C.M.G.
Mr. O. Harrison Williams
COMMITTEE
Vice-Chancellor H. J. W. Hetherington, |
M.A., LL.D. j
Mr. H. Wade Deacon, C.B.E. i
Associate Professor W. J. Billing ]
Professor ]. M. Beattie, M.A., M.D., )
C.M., M'.R.C.S., L.R.C.P. [
ProfessorW. Ramsden, M.A., D.lVr., B.Ch. j
Mr. Enfield E. Fletcher
Mr. J. N. Sellers
Mr. Cecil Bates
Mr. G. Brocklehurst
Mr. J. R. Danson
Mr. H. D. Dickie
Mr. R. D. Holt
Mr. David Jones
Mr. J. Pickering Jones
Mrs. Percy F. Kipung
Mr. R. Rankin
Mr. J. H. Sharrock
Mr. O. Harrison Williams
Professor W. Yorke, M.D., M.R.C.P.
Professor D. B. Blacklock, M.D.
Professor W. S. Patton, M.B.
University of Liverpool
Council of University of TJverpool
Senate of University of Liverpool
Royal Southern Hospital
Steamship Oimiers' Association
Shipowners A ssociation
Mr. J. A. Tinne, M.P., Hon. Treasurer
Mr. J. L. McCarthy, Secretary, C 17 — 18 Exchange Buildings, Liverpool
Dr. J. Middlemass Hunt, Hon. Dean, School of Tropical Medicine,
Pembroke Place, Liverpool
Staff, 1929
Alfred Jones Professor of
Tropical Medicine . . WARRINGTON YORKE, M.D., M.R.C.P.
Dutton Memorial Professor oi
Entomology . . . . WAI.'l'ER SCOTT PATTON, M.B.
IV alter Myers Professor of
Parasitology . . . \’acant.
Professor of T ropical Diseases of
Africa .... DONALD BREADALBANE BLACKLOCK, M.D.
Lecturer on Entomology . . ALWEN M. EVANS, M.Sc.
Assistant Lecturer on Entomology . Vacant.
Lecturer on Protozoology . . A. R. D. ADAMS, M.D.
Assistant Lecturer in Protozoology . FREDERICK. MURGATROYJ), M.B.
Lecturer on Helminthology . . . T. SOUTHWELL, D.Sc., F.R.S.E.
Clinical Pathologist . . D. UVEDALE OWEN, M.D.
Hon. Lecturer on Clinical
J^eterinary Parasitology . . A. W. NOEL FILLERS, F.R.C.V.S. '
Lecturer on Tropical Surgery . ROBER'F ERNEST KELLY, C.B., F.R.C.S.
Lecturer on Tropical Hygiene . A. J. IL RUSSFJ.L, Llout-Col. I.M.S., C.B.E., M.A., M.D., D.P.H.
Director of Museum . . . ROBERT NEWSTEAD, F.R.S.
Royal Infirmary, Liverpool
Physician . . . WARRINGTON YORKE, M.D., M.R.C.P.
Assistant Physician , . . Vacant.
Clinical Pathologist . . . D. UVEDALE OWEN, M.D.
Consulting Surgeon . . ROBER T ERNEST KELLY, C.B., F.R.C.S.
The Manaos Research Laboratory
Director HAROLD WOLFERSTAN THOMAS, M.D., C.M.
Sierra Leone Research Laboratory
Director .... DONALD BREADALBANE BLACKLOCK, M.D.
Assistant Director . . . RUPERT MONTGOMERY GORPON, M.D.
Research Assistants . . , J. FINE, M.B.
MARION WATSON, M.B.
T. H. DAVEY, M B.
E. P. HICKS, M.B.
VI
THE MARY KINGSLEY MEDAL
This medal was struck in commemoration of the work of the late
Miss Mary Kingsley in West Africa, and is conferred in recognition
of distinguished scientific achievement.
HONORARY RECIPIENTS
Her Royal Highness Princess Christian
J.ord Lister
The Right Hon. Joseph Chamberlain
Prince August e d’Arenberg
Mrs. Pinnock
Mr. William Adamson
Professor W illiam Carter
RECIPIENTS
1903 —
Colonel Sir David Bruce, K.C.B.
Geheimrath Professor Robert Koch
Dr. A. Laveran
Sir Patrick Manson, K.C.M.G.
1907 —
Professor Danielewsky
Dr. Charles Finlay
Mr. \V. M. Haffkine
Professor Golgi
Colonel Gorgas
Professor Theobald Smith
1910 —
Sir William Macgregor, G.C. M.G.
Professor R. Blanchard
Dr. Anton Breinl
Professor Angelo Celli
Dr. C. W. Daniels
Surgeon-General Sir Alfred Keogh
Colonel W. G. King
Professor Nocht
Professor G. H. F. Nuttall
Major Leonard Rogers
Professor J. L. Todd
Surgeon-General Walter Wyman
1913 —
Professor Fred V. Theobald
1917 —
Dr. Griffith Evans
1919 —
Dr. J W’. Scott Macfie.
The Oswaldo Cruz Institute, Rio de
Janeiro
1920 —
Major E. E. Austen, D.S.O.
Dr. A. G. Bagshawe, C.M.G.
Dr. Andrew Balfour, C.B.
Dr. A. L. G. Broden
M^rs. Chalmers, in recognition of the
work of the late Dr. A. J. Chalmers
Professor B. Grassi
Professor R. T. Leiper
Professor F. Mesnil
Dr. Edmond Sergent
Dr. C. W. Stiles
Dr. T. Zammit
Vll
THE ALAN H. MILNE MEDAL
This medal was struck to commemorate the late Alan H. Milne,
C.M.G., the first Honorary Secretary of the School (1899-1917), and
is awarded twice yearly on the recommendation of the examiners
for the Diploma in Tropical Medicine.
George Phillip Farmer Allen
Quintin Stewart
1923 --
John Cecil Cruickshank
1926 —
John McPhail Campbell
Triloki Nath Varma
1927 —
Alexander M. Gillespie
Joseph Hector Pottinger
Ragade Sanjiva Rao
1924 —
George Maclean
Frederick John Carlyle Johnstone
Bernard Langridgc Davis
1925 —
Khwaja Samad Shah
Alfred Robert Davies Adams
Alfred J. Hawe
1928 —
Joseph Fine
1929 —
Ian Cameron Middleton
Vlll
NOTICE
The following courses of instruction are given by the Liverpool
School of Tropical Medicine each year : —
(1) Two courses for the Diploma in Tropical Medicine,
commencing on the ist October and the 7th January.
The D.T.M. examinations are held in December and
March.
(2) Two courses for the Diploma in Tropical Hygiene,
commencing on the loth January and the 2-|th April.
The D.T.H. examinations are held in March and July.
(3) Two courses in Veterinary Parasitology, commencing on
Tst October and the 7th January.
DIPLOMA IN TROPICAL MEDICINE
This Diploma shall be awarded only to candidates who possess
a qualification to practise Medicine recognised for this purpose b}^
the University, and who present satisfactory certificates of having
attended approved courses of study, and pass the prescribed
examination.
DIPLOMA IN TROPICAL HYGIENE
This Diploma can only be taken by those who have already
obtained the D.T.M.
‘ The course for this Diploma will not be conducted unless
at least five applications are received, and no application for
admission can be considered later than December 21st and
March 3Tst respectively.'
FEES
D.T.M. Course
D.T.H. Course
Course in Veterinary Parasitology
Each Diploma Examination
. . . Twenty Guineas
... Ten (iiiineas
... Fifteen Guineas
... ETve Guineas
Fee for use of a School microscope 'during one term ... One Guinea.
For prospectus and further information, application should be
made to the Hon. Dean, School of Tropical Medicine, University of
Liverpool.
The following have obtained the Diploma in rropical Medicine
of the University of Liverpool : —
Diploma in Tropical Medicine
Date of
Diploma
1904 Augustine, Henry Joshua
1904 Bennett, Arthur King
1904 Bruce, VVilliam James
1904 Byrne, John Scott
1904 Clayton, Thomas Morrison
1904 Dalziel, John McEwen
1904 Dee, Peter
1904 Greenidge, Oliver Campbell
190^ Hehir, Patrick
1904 Khan, Saiduzzafor
1904 Laurie, Robert
1904 Maclurkin, Alfred Robert
1904 McConnell, Robert Ernest
1904 Nicholson, James Edward
t904 Philipson, Nicholas
1904 Sharman, Eric Harding
1904 Thomspn, Frank Wyville
1904 Walker, George Francis Clegg
1905 Anderson, Catherine Elmslie
1905 Brown, Alexander
1905 Caldwell, Thomas Cathcart
1905 Critien, Attilio
1905 Hooton, Alfred
1905 Hudson, Charles Tilson
1905 Illington, Edmund Moritz
1905 Macfarlane, Robert Maxwell
1905 Maddock, Edward Cecil Gordon
1905 Moore, James Jackson
1905 Nightingale, Samuel Shore
1905 Radcliffe, Percy Alexander Hurst
1905 Voung, John C'ameron
1906 Adie, Joseph Rosamond
1906 Arnold, Frank Arthur
1906 Bate, John Brabant
1906 Bennetts, Harold Graves
1906 Carter, Robert Markham
1 906 Chisholm, James Alexander
1906 Clements, Robert William
1906 Dundas, James
1906 Faichnie, Norman
1906 TefFreys, Herbert Castelman
1906 Mackenzie, Donald Francis
1906 Pailthorpe, Mary Elizabeth
1906 Palmer, Harold Thornbury
1906 Pearse, Albert
19^6 Sampey, Alexander William
1906 Smithson, Arthur Ernest
1906 Tayfor, Joseph van Someron
1906 Taylor, William Irwin
1906 Tynan, Edward Joseph
1906 Watson, Cecil Francis
1906 Willcocks, Roger Durant
1906 Williamson, George Alexander
1907 Allan, Alexander Smith
1907 Allwood, James Aldred
1907 Bond, Ashton
1907 Branch, Stanley
Date of
Diploma
1907 Collinson, Walter Julius
1907 Davey, John Bernard
1907 Donaldson, Anson Scott
1907 Fell, Matthew Henry Gregson
1907 Gann, Thomas William Francis
1907 Graham, James Drummond
1907 Hiscock, Robert Carroll
1907 Keane, Joseph Gerald
1907 Kennan, Richard Henry
1907 Kenrick, William Hamilton
1907 Le Fanu, George Ernest Hugh
1907 Mackey, Charles
1907 Maddox, Ralph Henry
1907 McCarthy, John McDonald
1907 Raikes, Cuthbert Taunton
1907 Ryan, Joseph Charles
1907 Vallance, Hugh
1908 Caverhill, Austin Mack
1908 Crawford, Gilbert Stewart
1908 Dalai, Kaikhusroo .Rustomji
1908 Dansey-Browning, George
1908 Davidson, James
1908 Dickson, John Rhodes
1908 Dowdall, Arthur Melville
1908 Glover, Henry Joseph
1908 Greaves, Francis Wood
1908 Goodbody, Cecil Maurice
1908 Harrison, James Herbert Hugh
1908 Joshi, Lemuel Lucas
1908 Le Fanu, Cecil Vivian
1908 Luethgen, Carl Wilhelm Ludwig
1908 Mama, Jamshed Byramji
1908 McCay, Frederick William
1908 McLellan, Samuel Wilson
1908 Pearce, Charles Ross
1908 Schoorel, Alexander Frederik
1908 Smith, John Maegregor
1908 Stewart, George Edward
1908 Tate, Gerald William
1 90S Whyte, Robert
1909 Abercrombie, Rudolph George
1909 Allin, John Richard Percy
1909 Armstrong, Edward Randolph
1909 Barrow, Harold Percy Waller
1909 Beatty, Guy
1909 Carr- White, Percy
1909 Chevallier, Claude Lionel
1909 Clark, William Scott
1909 Cope, Ricardo -
1909 Fleming, WilKam
1909 Hanschell, Mother McCormick
1909 Hayward, William Davey
1909 Henry, Sydney Alexander
1909 Innes, Francis Alexander
1909 Jackson, Arthur Frame
19P9 Kaka, Sorabji Manekji
1909 McCah^-Dallas, Alfred Alexander Donald
X
Date of
Diploma
1909 Meldrum, William Percy
1909 Murphy, John Cullinan
1909 Samuel, Mysore Gnananandaraju
1909 Shroff, Kawasjee Byramjee
1909 Thornely, Michael Harris
1909 Turkhud, Violet Ackroyd
1909 Webb, William Spinks
1909 Yen, Fu-Chun
1910 Brabazon, Edward
1910 Castellino, Louis
1910 Caulcrick, James Akilade
1910 Dowden, Richard
1 9 10 Ilaigh, \Villiam Edwin
1910 Hamilton, Henry Fleming
1910 Hefferman, William St, Michael
1910 Hipwell, Abraham
1910 Homer, Jonathan
1910 Houston, William Mitchell
1910 James, W^illiam Robert Wallace
1910 Johnstone, David Patrick
1910 Korke, Vishnu I'atyaji
1910 Macdonald, Angus Graham
1910 Macfie, John Wm. Scott
1910 Manuk, Mack Walter
1910 Murison, Cecil Charles
1910 Nanavati, Kishavlal Balabha
1910 Nauss, Ralph Welty
1910 Oakley, Philip Douglas
1910 Pratt, Ishmael Charles
1910 Sabastian, Thiruchelvam
1910 Shaw, Hugh Thomas
1910 Sieger, Edward Louis
1910 Sousa, Pascal John de
1910 Souza, Antonio Bernardo de
1910 Waterhouse, John Howard
1910 White, Maurice Forbes
1911 Blacklock, Donald Breadalbane
1911 Brown, Frederick Forrest
1911 Chand, Diwan Jai
191 1 Holmes, John Morgan
1 91 1 levers, Charles Langley
1911 lies, Charles Cochrane
1911 Ingram, Alexander
191 1 Kirkwood, Thomas
19 1 1 Knowles, Benjamin
19H Liddlc, George Marcus Berkeley
1911 Lomas, Emanuel Kenworthy
191 1 Mackarcll, William Wright
191 1 MacKnight, Dundas Simpson
191 1 Mascarenhas, Joseph Victor
1911 Murray, Ronald Roderick
191 1 Oluwole, Akidiya Ladapo
191 1 Rao, Koka Ahobala
191 1 Sinton, John Alexander
191 1 Tarapurvalla, Byramji Shavakshah
1911 Taylor, John Archibald
191 1 Woods, William Medlicott
1912 Acria, Joseph Reginald
1912 Anderson, Edmund Litchfield
1912 Boric, James
1912 Bowie, John Tait
1912 Brassey, Laurence Percival
Date of
Diploma
1912 Christie, David
1912 Dillon, llenry de Courcy
1912 Dunn, Lillie Eleanor
1912 Hardwicke, Charles
1912 Jagose, Jamshed Rustomji
1912 Kochhar, Mela Ram
1912 McGusty, Victor William Tighe
1912 Milne, Arthur James
1912 Mitra, Manmatha Nath
1912 Myles, Charles Duncan
1912 Pelly, Huntly Nevins
1912 Prasad, Bindeshwari
1912 Prentice, George
1912 Ross, Frank
1912 Russell, Alexander James Hutchison
1912 Ruthven, Morton Wood
1912 Sandilands, John
1912 Scddon, Harold
1912 Smalley, James
1912 Strickland, Percy Charles Hutchison
1912 Watson, William Russel
1913 Austin, Charles Miller
1913 Banker, Shiavux Sorabji
1913 Becker, Johann Gerhardus
1913 Carrasco, Milton
1913 Clark, James McKilllcan
1913 Forsyth, Charles
1913 Grahame, Malcolm Claude Russell
1913 Grieve, Kelburnc King
1913 Hargreaves, Alfred Ridley
1913 llepper, Evelyn Charles
1913 Hiranand, Pandit
1913 Jackson, Oswald Egbert
1913 Khaw, Ignatius Oo Kek
1913 MacKelvie, Maxwell
1913 MacKinnon, John MacPhail
1913 Macmillan, Robert James Alan
1913 Mouat-Biggs, Charles Edward Forbes
1913 Noronha, John Carmel
1913 O’Connor, Edward
1913 Olubomi-Bcckley, Emanuel
1913 Pestonji, Ardeshir Behramshah
1913 Puttanna, Dodballapur Sivappa
1913 Reford, John Hope
1913 Smith, Edward Arthur
1913 Stewart, Samuel Dudley
1913 Walker, Frederick Dearden
1913 Wilbe, Ernest Edward
1913 Wilson, Hubert Francis
1913 Yin, Ulg Ba
1913 Young, William Alexander
1914 Arculli, Hassan el
1914 Chohan, Noormahomcd Kasembha
1914 Connell, Harry Bertram
1914 Gerrard, Herbert Shaw
1914 Gimi, Hirji Dorabji
1914 Gwynne, Joseph Robert
1914 Hodkinson, Samuel Paterson
1914 Jackson, Arthur Ivan
1914 Kaushash, Ram Chander
1914 Kelsall, Charles
1914 Luanco y Cuenca, Maximino
1914 Misbah, Abdul-Ghani Naguib
XI
Date oj
Diploma
1914 Naidu, Bangalore Pasupulati Balakrishna
1914 Rowe, John Joseph Stephen
1914 Roy, Raghii Nath
1914 Shiveshwarkar, Ramchandra Vishnu
1914 Siir, Sachindra Nath
1914 Talati, Dadabhal Cursedji
1914 Wilkinson, Arthur Oeden
1914 Wright, Ernest Jenner
1915 Lobo, John Francis
1915 Madhok, Gopal Dass
1915 Pearson, George Howorth
1915 Swami, Karumuri Virabhadra
1915 Wood, John
1916 Barseghian, Mesroob
1916 Chaliha, Lakshmi Prasad
1916 Lim, Albert Liat Juay
1916 Lim, Harold Liat Hin
1916 Metzger, George Nathaniel
1916 Sdderatrom, Erik Daniel
1916 Wheeler, Louis
1917 Chapman, Herbert Owen
1917 Krishnamoorthy, Yedatore N^enkoba
1917 Lipkin, Isaac Jacob
1918 Watts, Rattan Claud
1919 Bowle-Evans, Charles Harford
1919 Burnie, Robert McColl
1919 Celcstin, Louis Abel
1919 Cummings, Eustace Henry Taylor
1919 Darling, Georgina Renington
1919 Drake, Joan Margaret Fraser
1919 Fraser, William James
1919 Gordon, Rupert Montgomery
1919 Krige, Christian Frederick
1919 Maplestone, Philip Alan
1 919 Oluwole, Isaac Ladipo
1919 Rustomjec, K-husshuyee Jamesidjee
1 9 19 Sawers, William Campbell
1919 Thompson, Mary Georgina
1919 Turner, Gladys Maude
1919 Young, Charles James
1920 Adler, Saul
1920 Anderson, William Jenkins Webb
1920 Campbell, George
1920 Cobb, Charles Eric
1920 Cobb, Enid Margaret Mary
1920 Conttolly, Evelyn Mary
1920 Fernandez, Daniel David
1920 Lim, Chong Eang
1920 McHutcheson, George Browne
1920 van der Merwe, Frederick
1920 O’ Farrell, Patrick Theodore Joseph
1920 Renner, Edo wo Awunor
1920 Vaughan, James Churchwill
1920 Waller, Harold William Leslie
1921 Allen, George Phillip Farmer
1921 Corhdd, Charles Russell
1921 Hamid, Abdul
1921 Longhurst, Bell Wilmott
1921 Maevae, George Anthony
1921 Madan, Hans Raj
1921 Mulligan, William Percival
Date of
Diploma
1921 Nixon, Robert
1921 Richmond, Arthur Stanley
1921 Shri Kent, Shamsher Singh
1921 Skinner, James Maegregor
1921 Stewart, Robert Bell
1921 Thomson, Marion
1922 Bhatia, Jagat Ram
1922 Cohen, Morris Joshua
1922 Crawford, Andrew Clemmey
1922 Gilmore, Edward Raymond
1922 Gracias, Cajetan Manuel
1922 Jennings, Arthur Richard
1922 l>ethem, William Ashley
1922 Paul, Sachchidananda IToshcn
1922 Pinder, John
1922 Ricley, Stanley Desmond
1922 Rutherford, Gladys
1922 Stewart, Quintin
1923 Abelman, B.
1923 Basu, Dhirendranath
1923 Cruickshank, John Cecil
1923 Doherty, Winifred Irene
1923 Edghill, Winifred M,
1923 Elsohn, John
1923 Fraser, N. D. .
1923 Lee, R.
1923 Pierce, E. R.
1923 Raja, Rojaporum
1923 Reid, C. B. B.
1923 Richmond, A. E.
1923 Steven, J. B.
1923 White, Charles Francis
1924 Bilimoria, H. S.
1924 Carson, J. C.
1924 Chopra, B. L.
1924 Davis, B. L.
1924 Hardy, M. J,
1924 Jennings, C. B.
1924 Johnstone, F. J. C.
1924 Keirans, J. J.
1924 Lee, S. W. T.
1924 Macdonald, G.
1924 Maclean, G.
1924 Mathur, W. C.
1924 Mitchell, J. M.
1924 Owen, D. Uvedale
1924 Palmer-Jones, Beryl
1924 Sankeralli, E. J.
1924 Singh, H.
1924 Theron, Elizabeth M,
1925 Adams, Alfred Robert Davies
1925 Ashton, Frank Richard
1925 Ashworth, Esther
1925 Bamford, Charles Walker
1925 Beinashowitz, Jack
1925 Black, John
1925 Clark, George
1925 Coghlan, Bernard A.
1925 Collier, Ivy
1925 Crawford, E. J.
1925 Cumming,^ Patrick Grant
xii
Data of
Diploma
1925
Eliam, Mary Muriel
Date of
Diploma
1926
Rodrigues, N.
192s
Fiiher, Morris
1926
Sachdev, A. S.
1925
Orcen, Frederick Norman
1926
Singh, B.
Singh, J.
1925
Grutu, M. S.
1926
1925
Hawc, Albert J.
1926
Talib, S. A.
1925
Jafri, Z. H.
1926
Tan, C. L.
19*5
Johnstone, Elvy I.
1926
Taylor, Catherine F.
1925
Kerr, James R.
1 926
T'urnbull, N. S.
1925
Mackay, Donald M.
1926
Turner, J. CL S-
1925
Mackay, E. K.
1926
V^ardya, B. K.
1925
Makkawi, M.
1926
Variua, T. N.
* 9*5
Maldonado, Leopoldo Oarcia
1926
Voigt, C.
1925
Mar, Severe Francisco
1926
Wasti, S. N.
1925
19^5
Mozoomdar, B. P.
Shah, KLhwaja Samad
1927
Allen, P.
J925
Skan, Douglas A.
1927
Bahl, M. T..
J925
Stone, Ernest R.
1927
Barrowinan, B.
1925
Terrell, C. G.
1927
Bawa, H. S.
1925
Tooth, Frederick
1927
Bilirnoria, j. D.
1925
de Waal, Jacobus Johannes
1927
Burns, W.‘M.
1926
Aitken, W. J.
1927
1927
Daly, E. J.
Dunlop, CL A.
1926
Ashworth, A.
1927
Dyrcani, V.
1926
Austin, T. A.
1927
Evans, R. R.
1926
Bansikar, R. N.
1927
P’arid, M.
1926
Besson, W. W.
1927
GiUcspic, A. M.
1926
Bligh-Pcacock, R. N.
1927
C.unawardana, S. A.
1926
Bolton, EHic Ch
1927
flarkncss,
1926
Boodrie, E. 1 1.
1927
1 lay, R.
1926
Brito-Mutuna yagain, M. A. B.
1927
Jlodivala, N. JV1.
1926
Campbell, J. McP.
1927
1 lughes, Emma
1926
Cullen, T.
1927
Ilyslop, Kathleen M.
1926
I>avie8, H. E.
1927
Tngram-Johnson, R. E.
1926
Dias, B. G. V.
1927
Kapadia, J. S.
1926
Doherty, H. A. A.
1927
Khan, I". A.
1926
Don, E. G.
1927
Khan, M. M.
Lahuschagne, P. N. 11
1926
Earl, J. C. St. G.
1927
1926
Fletcher, Beatrice N.
1927
Laird, W. J.
1 926
Fowler, H. P.
1927
Lewin, B. F.
1926
Fowler, Isabella J,
1927
Macdonald, J.
1926
Hamilton, J.
1927
McElroy, R. S.
1926
llodgkinson, Katharine IVl.
1927
Maclay, W. S.
1926
Jackson, R.
1927
Maguire, IL CL
1926
Kamakaka, K.. H.
1927
Mahaffy, A. F.
1926
Kennedy, J. H-
1927
Malliotra, A. 1 1.
1926
Khatri, L. D.
1927
Malhotra, A. L.
1926
Lennox, D.
1927
Ailanghirmalani, B. S.
1926
Lewis, A. J.
1927
Meek, A. I.
1926
McConn, C. F.
1927
Mehra, J. N.
1926
Mackay, A. G.
1927
Mehta, II. C.
1926
McLean, N-
1927
Menon, M. V.
1926
MaeSweeney, M.
1927
Miller, H. V. R.
1926
Malhautra, K. L.
1927
Mokand, S. N.
1926
Malik, S. B.
1927
Murgatroyd, F.
1926
Manuwa, S. L. A.
1927
Murray, A. J.
1926
Merchant, M. E.
1927
Murray, Pauline V.
1926
Mitchell, W. H.
1927
Nevin, IL M.
1926
Molony, E- F.
1927
Nirula, P. N.
1926
Nashikkar, S. G,
. *927
Olusoga, N.
1926
Oppenheimer, F.
1927
Parakh, D. B.
1926
Ormiston, W. S.
1927
Peters, D. O.
1926
Paterson, F. S.
1927
Peters, M. R.
1926
Patterson, F- L.
1927
Pottinger, J. H.
1926
Pouri, V.
1927
Rao, R. S.
1926
Quigley, L, D.
1927
Rodriguez, C». S.
1926
Robertson, A.
1927
Shah, S. R. A.
xiii
D^e of
Difioma
Date of
Diploma
Mitchell, A.
Singh, 11 .
1928
1917
Southward, J. F.
1928
Mone, R. V.
! 9 Z 7
Sturton, S. J>.
1928
Morley, A. H.
i<)i 7
Thompson, Frances C.
1928
Mo.stert, If. van R.
1927
de Villicrs, B. J. van de S.
1928
Mufty, S.
1927
Walklnshaw, R.
1928
van Niekcrk, S. V.
1927
Wilkinson, S. A.
1928
1928
Pandit, M. K,
Pearce, W. T. A.
1928
Ahluwalia, C. L.
1928
Plum, I).
1928
Aidin, A. R.
1928
Rao, B. D.
1928
Anand, J. S.
1928
Reid, A.
19-'8
Askari, S. W. H.
1928
Sanderson, 1 .
1928
Beveridge, Ruby S.
1928
Setna, 11 . M.
1928
Biswas, M. K.
1928
Shearer, G.
1928
Blakemore, W. L.
1928
Singh, B.
r928
Camps-Carnpins, J. M.
1928
Sivalingam, S.
1928
Chacko, M. O.
1928
Stratton, Ella M.
1928
Chopra, A. N.
1928
Suri, R.
Tuli, R. L.
1928
Chaudhuri, J. P.
1928
1928
Choudari, K. V. R.
1928
Udvadia, F. F.
1928
Cranage, Margaret
1928
Waglc, P. M.
1928
Dhala, C. n.
1928
Wahid, A.
1928
Dhar, K. K.
1928
Wall-Mcshani, Nellie
1()28
1928
Oikshit, 11. K.
Kverard,'N. J.
1928
Whig, P. L.
1928
Fine, J.
1929
Chakravarti, K. B.
1928
(Jhei, A. N.
1929
Crawford, J.
1 928
Ilalawani, A.
1929
Dale, W. C.
Dogra, R.
1928
Henshaw, L. E. R.
1929
1 928
llilmy, J. S.
1929
Drury, G. I).
1928
Holmes, W. E.
1929
Gill, T. S.
1928
Hope-Gill, C, W.
1929
llerbcrtson, Margaret A. L.
1928
Kane, F.
1929
Innes, J. A. L.
1928
Katial, C. L.
1929
McGregor, J. A.
1928
Khan, F. M.
1929
McQueen, W. B.
1928
Krishna, R,
1929
Majumdar, B. K.
1 928
Lawrence, 11 . S.
1929
Middleton, I. C.
1928
Lawrence, M. R.
1929
Pearse, J. 1 '. IL
1928
McLaren, D. W.
1929
Ramdeholl, C.
1928
Malhotra, B. D.
1929
Robinson, Elizabeth J.
1928
Mallick, IL D.
Mason, Jean R.
1929
Robinson, P. fi.
1928
1929
Shafi, A.
1928
Menon, E. S. R.
1929
Verghese, 1 '.
1928
Milne, J.
1929
Wilson, S. P.
The following have obtained the Diploma in Tropical Hygiene
of the University of Liverpool : —
Diploma in Tropical Hygiene
Dat€ of
Diploma
1926
Aitkcn, W. J.
Bligh'Peacbck, N.
Date of
Diploma
1926
MaeSweeney, M.
1926
1926
Oppenheimer, F.
1926
Clark, G.
1926
Skan, D. A.
1926
Collier, Ivy
1926
Talib, S. A.
1926
Cullen, T.
1926
Turnbull, N. S.
1926
Davis, B. L.
1926
Don, E. G. A.
1927
Allen, C. P.
1926
Fowler, H. P.
1927
Austin, r. A.
[926
Hawe, A. J.
1927
Besson, W. W.
1926
Lennox, D.
Mackay, A. G.
1927
Dunlop, G. A.
1926
1927
Earl, J. C. St. G.
1926
Mackay, D. M.
1927
Hamilton, J.
1926
McLean, N.
* 9^7
Harkness, J.
XIV
Bate of
Diplmna
1927 Hay, R.
1927 Hy»lop, Kathleen M.
1927 Labuschagnc, P. N. H.
1927 McCon, C. F.
1927 Macdonald, J.
1927 Mitchell, Winifred H.
1927 Murray, A. J.
1927 Nevin, H. M.
1927 Nixon, R.
1927 Ormiston, W. S.
1927 Robertson, A.
1927 Walkingshaw, R.
1928 lUlimoria, J. I).
1928 Blakemorc, W. L.
1928 Choudaii, K. \'. R.
1928 Dhar. K. K.
Date of
Diploma
1928 Evans, R. R.
1928 llolmcR, W. E.
1928 Laird, W. F.
1928 Maclay, W. S.
1928 Miller, II. V. R.
iq28 Morlcy, A. H.
1928 Pearson, G. II.
1928 Pottinger, J. II.
1928 Sanderson, 1.
1928 Sivalingani, S.
1928 Wilkinson, S. A.
192<) Askari, S. W. II.
1921) llalawani, A.
1929 Ailniy, 1 . S.
1929 Lan'roncf, H. S.
1929 Setna, 11 . M.
XV
ANNALS OF TROPICAL MEDICINE
AND PARASITOLOGY
EDITORIAL NOTICE
Articles for publication should not exceed twenty-five pages of
the Annals, and will be understood to be offered alone to this
Journal. They should be typewritten and addressed to : — The
Editors, School of Tropical Medicine, The University, Liverpool.
Illustrations for text figures or charts should be drawn clearly
and firmly in Indian ink, if possible on Bristol board. N.B . — Blue
or other coloured ruling in squares or lines cannot be reproduced.
All lettering, names or legends on text-figures, charts or maps
should be printed sufficiently large to allow of clear legibility on
reduction if necessary.
Plates and illustrations should be accompanied by short
explanations.
References to authors in the text must be made in the following
way : — ' According to Smith (1900) the spleen is enlarged, but
Robinson {1914) says the reverse.' The references should be
collected in alphabetical order of authors' surnames at the end of
the paper, and arranged in the following way : —
Kobinson, S. (1914), The spleen in malaria. Ann. of Nosology,
20 , 20-25.
Smith, J. (1900). Enlargement of the spleen in malaria. Jl. of
Pathomelry, 1 , 1-20.
Twenty-five reprints are supplied of each paper,
free of charge. Additional copies (up to 100) can be supplied at
cost price.
Subscription : 2s. 6d. per volume, post free, payable in
advance to The University Press of Liverpool, 177 Brownlow
Hill, Liverpool, to whom correspondence concerning advertisements
should also be addressed.
XVI
STUDIES ON THE TREMATODE— FAMILY
HETEROPHYIDAE
BY
G. WITENBERG
(From the Department of Parasitology , The Hebrew University,
Jerusalem)
(Received for publication 20 May, 1928)
CONTENTS
I. Introduction
II. General Remarks on the Life-Cycle of the Heterophyidae
III. General Remarks on the Classification of the Heterophyidae
History of the family
Structure of the genital pore of the Heterophyidae
Diagnosis of the family
Contents of the family
Methods of classification ...
List of species
IV. Classification and Life-History of the Heterophyidae :
Sub-family Heterophyinae ... ...
Key to the genera of the sub-family Heterophyinae
History of the genus Heterophyes
Diagnosis of the genus Heterophyes
Life-history of the members of the genus Heterophyes
Morphology of the metacercariae
Development of Heterophyes in the final host
Remarks on the morphology of adults
Morphology and classification of the species of the genus Heterophyes
Occurrence of Heterophyes species
Genus Metagonimus
Genus Dexiogonimus
Genus Diorchitrema
Genus Stictodora ...
Genus Galactosomum
Genus Microlistrum
Genus Crypiocotyle
Genus Tocotrema
Genus Rossicotrema
Genus Apophallus
Sub-family Centrocestinae
Key to the genera
Genus Pygidiopsis
Genus Parascocotyle
Sub-family Cercarioidinae
Genus Cercarioides
Sub-family Haplorchinae
Genus Haplorcbis
Genus Monorcbitrema
Sub-family Adleriinae
Genus Adleria
V. Reference List of the Bibliography of the Family Heterophyidae
VI. Summary
PAGE
... nz
- *33
... 134
... 134
... 134
... 136
- *37
... 138
... 140
... *43
... 143
... 144
... 146
... 147
... 149
... 151
*53
... *55
... 168
169
... 170
••• *73
... 176
*79
*79
180
iSi
182
183
184
184
*85
187
... 197
... 197
... 200
... 200
... 200
... 206
... 206
... 209
- ^33
131
I. INTRODUCTION
The family Heterophyidae Odhner, and its individual members^
have repeatedly attracted the notice of many writers. Zoologists
have called attention to their peculiar anatomical structure, while
medical men have studied these worms because some of them are
parasites of man and domestic animals.
In spite of a rather large literature, including several mono-
graphs devoted to Heterophyidae, there still remain many obscure
points in their anatomical structure, life-history and classification.
In the present paper it is hoped to clear up the existing discrepancies
on the basis of investigations on the Palestinian representatives of
the Heterophyidae.
Palestine proved to be rich in Heterophyidae, for fourteen
members of this family have so far been found in the country.
Nine of them have already been described by different authors,
the remaining five proved to be new to science.
It is of interest to point out that while six out of the nine known
species have been found in neighbouring countries (Egypt and
Italy), the other three, namely Monorchitrema taihui Nishigori,
Monorchitrema taihokui Nishigori, and Parascocotyle longa (Ransom)
are described from the other hemisphere — the first two from
Formosa, the last from Alaska,
Material on which the present paper is based was collected from
animals caught in Jerusalem, Tel Aviv, and the vicinity of Tiberias ;
in addition animals, mainly dogs and cats, were infected experi-
mentally and the life-history in the final host studied.
Thus the intermediate hosts of the majority of these trematodes
were detected. Investigations on the earlier stages of Heterophyidae
have also been inaugurated but they require more time to be com-
pleted and the results will be published later.
The writer had the opportunity of using some cotype specimens
generously sent to him by Dr, W. Arndt from the Berlin Museum,
by Professor J. Ciurea from the University of Bucharest, by
Dr. L. Szidat from the Konigsberg Museum, and by Professor M, C.
Hall and Dr. A. Hassall from the Bureau of Animal Industry,
Washington.
The author takes this opportunity to express his gratitude to
all these gentlemen for their kindness.
133
n. GENERAL REMARKS ON THE LIFE CYCLE OF THE
HETEROPHYIDAE
The life-history of several species of Heterophyidae have already
been studied by different authors. It was found that cercariae
develop in snails. From the snail the cercaria reaches a fish, encysts
in the organs of the latter and becomes a metacercaria. The latter
after being swallowed by the final host gives rise to the adult worm,
which parasitises the intestine.
My experiments with Palestinian Heterophyidae confirmed this
general course of development which appears to be constant and
typical. I also convinced myself that the majority of species
are not specific in their choice of hosts. The metacercariae of
Heterophyidae may encyst in various fishes belonging not only to
different genera but also to different families. Similarly many
.species of Heterophyidae are not particular in their choice of a final
host as they may develop partially or completely in both mammals
and birds. A certain degree of specificity regarding the final host
has, however, been observed. Faust and Nishigori have already
pointed out that the species of the genus Monorchitrema may
develop in some final hosts only up to a certain degree, and are
then passed out. In my experiments, the metacercariae escaped
from their cysts in all laboratory animals, but while in some the full
development occurred and the worms reached maturity, in others the
Trematodes lived only a short time and passed out before reaching
maturity.
Further, even among the final hosts in which the worms can
reach maturity, some are more suitable than others. In the more
suitable hosts the parasites grow to a large size and produce many
eggs, in the others the development is feeble and the worms are
small. This phenomenon led the earlier investigators to misinterpret
the specific characters of Heterophyidae and to consider one species
as several according to the number of hosts in which it occurred.
In my experiments the Heterophyidae developed in dogs better
than in cats, in cats better than in rabbits. The same species found
in mammals are in most instances better developed than in birds.
As the development of Palestinian Heterophyidae is similar in
all species, a detailed description is given only for Heterophyes
heterophyes (Siebold), which may serve as a model. The cited
134
numbers of secondary hosts of particular species of Heterophyidae
should not be considered as complete, as only few out of very
numerous species of fishes occurring in Palestine were used for the
experiments.
III. GENERAL REMARKS ON THE CLASSIFICATION OF THE
HETEROPHYIDAE
History of the Family
The name Heterophyidae was given by Odhner (1914) to replace
the former incorrect names Cotylogonimidae and Coenogonimidae,
Odhner included in this family the genera which have been attributed
to it by previous authors and several others the systematic position
of which l^ad been uncertain. The first attempt to gather all known
species into a closed group was made by Ransom (1920), who gave
a new modified diagnosis but divided the family only into genera,
though the outlines of three sub-families had been already defined
by previous authors. Ciurea was the first who defined the division
of the Heterophyidae into sub-families. He differentiated the
following five sub-families : Heterophyinae, Metagoniminae, Centro-
cestinae, Apophallinae, and Cryptocotylinae, basing himself on the
structure of the terminal portion of the genital ducts. Later Faust
and Nishigori (1924) added a sixth sub-family — Monorchitreminae.
Meanwhile, Nicoll (1923) included the sub-families Microphallinae and
Gymnophallinae as well as some genera which up to this date have
not been attributed to it. Poche (1926) added several more famihes
and genera to the Heterophyidae, According to the latter author,
whose contribution summarises all the present knowledge of
Heterophyidae, this family should consist of very differently organized
forms which deviate considerably from the type genus.
Structure of the genital pore in Heterophyidae
A comparative study of the anatomical structure of various
members of this family led me to the conclusion that the peculiarities
and extent of this family require to be cleared up, the significance
of some of its typical characters must be defined and some genera
removed from it. The most typical, character of Heterophyidae is
135
the structure of the terminal portion of the genital ducts and the
genital aperture or so-called ' genital sucker/ The term ' genital
sucker ' is attributed by authors to rather dissimilar structures
which should be differentiated. In the genus Heterophyes this
organ is a large protrusible body which may be retracted into
a sac-like hollow which appears to be the homologue of the genital
sinus of other Trematodes. This complicated structure, unlike
the ventral sucker, possesses no adhesive functions and therefore the
term ' genital sucker ' seems to me to be a misnomer. I propose
to name the protrusible body ' gonotyl,' while the cavity into
which it may be retracted should be called ' genital sac,' as proposed
by Yokogawa, 1913. (Fig. 7.)
The genus Heterophyes is the only one of the family Heterophyidae
which has a ventral sucker independent of the genital sac. In
other genera the ventral sucker is more or less reduced or modified
and included in the genital sac, together with the gonotyl, which is
reduced proportionally to the development of the ventral sucker
(' Spharoider Korper ’ of Jagerskjold). All these structures form
together a peculiar organ for which the term ' ventro-genital
sac ' is proposed. In some genera in which the well-developed
gonotyl occupies the whole ventro-genital sac the ventral sucker
may disappear completely {Stictodora, Monorchitrema, etc.). In
other genera in which the ventral sucker is well developed the
gonotyl is reduced to a comparatively small muscular tubercle
{Pygidiopsis , etc.) or to two tubercles {Apophalliis , etc.).*
These tubercles have been observed by the earlier authors who
called them * lenticular shaped bodies,’ but their position has been
misinterpreted. They are situated not on the ventral surface of
the body, but inside the ventro-genital sac from which they may be
occasionally protruded.
While in the members of the genus Heterophyes the genital
aperture is situated on the top of the gonotyl, in other genera it
lies at the base of this organ. In the majority of species the gonotyl
bears chitinous spines, plates, bars,' etc., on its surface.
• The Heterophyidae are not the only Trematodes with such a coniplicated genital sinus.
Similar structures are also present in other groups of Trematodes, as for instance Microphallinae^
Hemiuridae^ Axygiidae^ etc.
136
Diagnosis of the Family Heterophyidae Odhner.
On the basis of material worked out in this paper together
with previous literature the family Heterophyidae may be defined
as follows :
Small and very small forms. Pseudodermis covered with
scale-like spines. The body is usually divided into two parts,
one anterior flattened, free from genitalia and more motile than the
posterior part which is oval or round in cross-section and contains
the genital apparatus. The oral sucker may be provided with all
or a part of the following structures : a contractile dorsal lip-like
appendage, a posterior funnel-shaped appendage and rows of
circumoral spines.
Praephar5mx and oesophagus vary in different genera and
species. Pharynx always present. Intestinal caeca simple, of
varying length. Ventral sucker, except in the genus Heterophyes,
reduced and included in the modified genital sinus (* ventro-genital
sac ’) or even absent.
The reproductive organs, except the vitellaria in some genera,
are grouped in the posterior part of the body behind the level of the
genital aperture which is generally situated near the middle of the
body. Testes, two or one, globular or lobed : their situation
varies in different genera. The cirrus pouch is absent. The seminal
receptacle is voluminous and may be divided into several parts by
constrictions. The terminal portion of the seminal vesicle may
form a separate vesicle-shaped organ which is usually provided with
chitinised walls ; the term * expulsor ' is proposed for this structure
(in Heterophyes, Tocotrema, Diorchitrema, etc.). Ovary globular or
slightly lobed and, except in Adleria, is situated in front of the
testes. MehUs' gland present. Seminal receptacle well developed.
Laurer’s canal usually reduced. The vitellaria are usually situated
near the lateral or dorsal surface of the body and the degree of their
development varies in different species. The uterus in most cases
does not proceed anteriorly to the genital aperture. The latter,
except in Heterophyes, opens on the inner wadi of the ventro-genital
sac, which is situated on the middle line or moved towards the
lateral border of the body. Near the genital aperture a more or less
developed gonotyl is often present. Eggs usually numerous with
157
thick* shell i8 to 37// long. Excretory vesicle usually Y-shaped ;
the length of the stem varies in different genera and it is either
straight, S-shaped or divided into branches which may re-unite (as in
Scaphanocephalus) ; the branches may be long, short or entirely
absent (as in Galactosomtim) .
Adults parasitise the intestines of mammals, birds, and rarely
fish {Haplorchis). Metacercariae encysted in fish. Cercariae,
as far as is known, develop in operculated molluscs.
Type genus : — Heterophyes Cobbold, 1866.
Contents of the Family.
On this new interpretation of the family Heterophyidae the
following sub-families and genera, which have been included in it by
NicoU and Poche, must now be excluded.
The genera united in the sub-family Microphallinae Ward, 1901,
do not belong to the HeterophyidaCy since they lack a seminal
receptacle and some of them are provided with a cirrus pouch.
The species united in the sub-family Gymnophallinae Odhner, 1905,
do not belong to the Heterophyidae because they lack a seminal
receptacle.
The genus Sigmapera Nicoll, in spite of its great resemblance to
Heterophyidaey cannot be assigned to this family because of its
well-developed cirrus pouch.
. The genus N anophyetus Chapin (in Hall, 1927) is characterised
by the presence of a well-developed cirrus pouch and does not
possess a seminal receptacle (of this I convinced myself after
examining the cotype specimens). It does not therefore belong to
Heterophyidae.
The genera Euryhelmis Poche, 1926, and Taphrogonymus Cohn,
1904, are based on insufficient descriptions of their representatives
and therefore there is no sufficient reason for including them in
the Heterophyidae.
The genera Parahascus Looss, 1907, and Cryptotrema Ozaki, 1926,
certainly do not belong to Heterophyidae.
The genus Paracoenogonimus Katsurada, 1914, appears to be
a synonym of the genus Prohemistomum Odhner, 1919, or Cyathocotyle
Miihling, 1896, which do not belong to Heterophyidae.
138
The genus Opisthometra Poche, 1926, belongs to Acanthochasmidae,
but not to Heterophyidae,
The genus Cladocystis Poche, 1926, should be relegated to the
Opisthorchidae until the genital pore of its members is re-described.
On the other hand, I include in Heterophyidae the genus Stictodora
Looss, 1899, which Poche has created an unnecessary family
Stictodoridae, relying on the incorrect description of Looss, and four
new genera: Dexiogonimus, Diorchitrema, Cercarioides, and Adleria*
It is probable that some of the genera and sub-families which
have been excluded from Heterophyidae in this paper will be assigned
to the super-family Opisthorchoidea after further investigations. On
the other hand, it is very probable that many known species which
arc at present included in other systematic groups will, after correct
re-descriptidn, be assigned to the Heterophyidae.
Method of Classification.
Since the above-mentioned genera are excluded from the
family Heterophyidae, the remainder should be distributed in sub-
families according to the method defined by Ciurea, i.e., according to
the details of the structure of the genital pore. But this method
has disadvantages, for in Heterophyidae, in contrast to other
Trematode families, the position and the structure of the genital pore
are very variable and proved to be valid only as generic characters.
On Ciurea's method one should create almost as many sub-families
as there are genera. Not the most changeable, but on the contrary,
the most constant features should be taken as a basis for division
into sub-families.
On investigating the comparative anatomy of known genera of
Heterophyidae it appeared that they may be readily arranged in
homologous rows, according to the principle of taxonomical
coeflftcients, which I have introduced for Cyclocoelidae (1926).
The following complex of features was found useful for a sub-
family coefficient, i.e., for characterising a sub-family.
(i) The shape of the anterior part of the body (dilated or not).
•The HtUrophyidae appear to be most closely related to the Opisthorchidae Liihc and both
form the nucleus of a new super-family Opisthorchoidea. They have a common scheme of anatomical
structure, both in adults and cercariae, and sin&ilar life-hiatxuries. They differ from each other mainly
in the structure of the terminal portion of the genital ducts and in that Heterophyidae parasitiie
the intesdne while OpitOtorebidae are found in tihe bile ducts of final hosts.
1.39
(2) The presence or absence of conspicuous spines round the oral
aperture, and
(3) The number of testes and their position in relation to the
ovary (in front or behind it).
The distribution of vitellaria may be regarded as a coefficient
of a tribe, i.e., it serves to distinguish tribes.
Various combinations of the following characters form a generic
coefficient : (i) the arrangement of the genital glands ; (2) the
structure and position of the ventro-genital sac ; (3) the additional
structures of the oral apparatus, and (4) where division into tribes
is not indicated, the distribution of the vitellaria.
All other peculiarities are specific characters.
On this scheme all existing genera of Heterophyidae may be
distributed among five sub-famihes : Heterophyinae Ciurea, 1924,
Centrocestinae Looss, 1899, C ercarioidinae n. subf., Haplorchinae
Pratt, 1902, and Adleriinae n. subf. These sub-families may be
determined on the following key :
A. Testes two :
(1) the anterior part of the body very dilated Cercarioidinae
(2) the anterior part of the body not dilated
{a) circumoral spines present Centrocestinae
ib) circumoral spines absent Heterophyinae
B. One testis :
(1) ovary in front of the testis Haplorchinae
(2) ovary behind the testis Adleriinae
Every sub-family could be divided into two tribes, according to
*the distribution of the vitellaria. In some genera the vitellaria are
confined to the region behind the level of the ovary, in others they
extend anteriorly beyond the genital aperture.
These features are observed in three of the five sub-families
and they may therefore be considered as homologous. In the
sub-family Heterophyinae, which has many genera, such a division
maybe useful, but in other sub -families, which contain comparatively
few genera, division into tribes is nqt yet necessary. It is probable
that when more genera are estabhshed, the division of all sub-
families of Heterophyidae into tribes will be practical.
As pointed out, the sub-family Heterophyinae is the richest in
genera and in it one observes the most diverse combinations of
features, which form the generic taxonomical coefficient, i.e., all
140
possible arrangements of the genital glands and various structures
of the ventro-genital sac.
The arrangement of the testes is the most noteworthy feature.
One can recognise three main dispositions : (i) testes lying side
by side, (2) obliquely to the long axis of the body, and (3) almost
along this axis. In addition, they may be situated at the posterior
extremity of the body or removed anteriorly ; thus six dispositions
of the testes exist. Each mode of arrangement of the testes may
be represented by several genera which differ from each other in
the position or structure of the ventro-genital sac and the distribution
of the vitellaria.
All the above six dispositions of the testes are possible in other
sub-families, but actually only some of them have been found so far.
If one arranges all the known genera of Heterophyidae in a table
in which those belonging to one sub -family are placed in longitudinal
rows and each space in the transverse direction corresponds to
a definite disposition of the testes, one receives a table of homologous
rows, in which the parallelism in the development of the features
in different sub-families of Heterophyidae is clearly seen. (See Table I.)
Many empty squares remain in this table — they wait for still
undescribed genera, the main features of which can easily be foretold.
List of Species
In the following list all species of Heterophyidae are arranged
according to the new classification. {* — Denotes those found in
Palestine.)
A. Heterophyinae Ciurea, 1924
{a) Heterophyea n. tr.
I. Diofchitrema n. gen.
•(i) D. pseudocirrata n. sp.
II. Dexiogonimus n. gen.
*(2) D, ciureanus n. sp.
III. Heterophyes Cobbold, 1866
•(3) H, aequalis Looss, 1902
*(4) H, dispar Looss, 1902
*(5) H. heterophyes (Siebold, 1852)
(6) H, nocens Onji, 1915
IV. Metagonimus Katsurada, 1912
(7) M, romanicus (Ciurea, T915)
(8) M, yokogawai (Katsurada, 1912)
Table I
I41
g
0
Aileriinae
Vltellaria Vitellaria
short long
1 : i
... Adleria
- ^
1
^ i
Haplcrcbinae
Vitellaria i Vitellaria
short ; long
Monorcbitrma
Haplorchu
Cercarioidinae
Vitellaria
long
f
i
CO
\
. Cercarioides
Vitellaria
short
Two Testes
Centrocestinae
J a
i>
li
•;>
Centrocestus
Ascocoiyle
Stamnosma
— -
Pygidiopsis
ParascocQtyle
Heteropbyinae
Vitellaria long
[Cryptocotylea]
Cryptocotyle
T ocotrma
Rossicotrema
>ja
1
Stictodora
Galactosomum
S
S
J
Vitellaria short
{Heteropbyea)
Diorchitrema
Dexiogonimus
Heteropbyes
^Metagonimus
V
T3
J S3
72
>>
•X3
.5 a3
TT
P
J-5
•j
ua
<u ^
g s
0
c
0
c^5
0
0
li
® ® i
fl'
S -o
-o rS
s I
^ X
0
.2
“O M -0
JW 0
rs-s
S -a M-
<2 S.°
142
V. Stictodora Looss, 1899
•(9) 5 . sawakinensis Looss, 1899
VI. Galactosomum Looss, 1899
(10) G. lacteum (Jagerskjold, 1896)
(11) G. erinaceum (Poirier, 1886)
VII. Microlistrum Braun, 1901
(12) M. cochlear (Diesing, 1850)
(13) M. cochlearijorme (Rudolphi, 1819)
(14) M. semijuscum (Olsson, 1876)
(15) M.spinetum (Braun, 1901)
{h) Cryptocotylea n. tr.
VIII. Cryptocotyle Liihe, 1899
(16) C. concavutn (Creplin, 1825)
(17) C. crypto cotyloides (IssaitshikoflF, 1923)
, (18) C. quinque angular e (Skrjabin, 1923)
IX. Tocotrema Looss, 1899
(19) T. (?) echinata (Linstow, 1878)
(20) T. jejunum Nicoll, 1907
(21) T. lingua (Creplin, 1825)
X. Rossicotrema Skrjabin, 1919
(22) R. donicum Skrjabin, 1919
XI. Apophallus Liilie, 1909
(23) A. muhlingi (Jagerskjold, 1899)
H. Centrocestinae Looss, 1899
XII. Pygidiopsis Looss, 1907
•(24) P. genata Looss, 1907
XIII. Parascocotyle Stunkard and Haviland, 1924
*(25) P, ascolonga n. sp.
*(26) P. italica (Alessandrini, 1906)
*(27) P, longa (Ransom, 1920)
(28) P. minuta (Looss, 1899)
(29) P. nana (Ransom, 1920)
(30) P. pithecophagicola (Faust, 1920)
XIV. Centrocestus Looss, 1899
(31) C. cuspidatus Looss, 1899
XV. Ascocotyle Looss, 1899
(32) A, coleostoma Looss, 1899
(33) A, agrense Travassos, 1916
XVI. Stamnosoma Tanabe, 1922
(34) S. armatum Tanabe, 1922
(35) S. formosanum Nishigori, 1924
C. Cercarioidinae n. subf.
XVII. Cercarioides n. gen.
*(36) C. aharonii n. sp.
XVIII. Scaphanocephalus Jagerskjold, 1903
(37) 5 . australis Johiiston, r9i7
(38) 5 . expansus (Creplin, 1842)
143
D. Haplorchinae Pratt, 1902
XIX. Monorchitrema Nishigori, 1924
•(39) M. taihokui Nishigori, 1924
*(40) M. taihui Nishigori, 1924
XX. Haplorchis Looss, 1899
(41) H, cahirinus (Looss, 1896)
(42) H, pumilio (Looss, 1896)
E. Adleriinae n. subf.
XXI. Adleria n. gen.
*(43) A, minutissima n. sp.
IV. CLASSIFICATION AND LIFE HISTORY OF THE
HETEROPHYIDAE
Sub-family Heterophyinae Ciurea, 1924.
Diagnosis : Heterophyidae with more or less flattened body, more
so anteriorly than posteriorly ; no dilation of the anterior extremity ;
no circumoral spines ; two testes situated behind the other reproduc-
tive organs.
Type genus : — Heterophyes Cobbold, 1866.
This sub -family may be divided into two tribes — Heterophyea and
Cryptocotylea.
Key to the genera of the sub-family Heterophyinae.
A. The vitellaria do not extend anteriorly beyond the level of the
ovary Tribe Heterophyea.
I. The testes are situated at the posterior extremity of the
body :
{a) the testes lie side by side :
(1) the ventro-genital sac is situated near the
middle Hne of the body Diorchitrema,
(2) the ventro-genital sac is situated near the
right border Dexiogonimus.
(b) the testes lie obliquely to the axis of the body ;
(1) the ventral sucker is separated from the genital
sac and lies at the middle line of the body ...Heterophyes.
(2) the ventral sucker is included in the ventro-
genital sac near the right border of the
body Metagonimus.
II. The testes are removed towards the middle of the body :
{a) the testes lie obliquely:
(1) the stem of the excretory bladder is S-sh.2i-p&d. . .Stictodora.
(2) the stem of the excretory bladder is Y -sh.2iped...Galactosomum
(b) the testes lie one behind the other Microlistrum.
144
B. The vitellaria extend anteriorly beyond the level of the genital
aperture Tribe Cryptocotylea.
I. The testes lie side by side ; the shape of the body is
almost round Cryptocotyle.
II. The testes lie obliquely to the axis of the body which is
oval or pyriform :
(^) one gonotyl in the ventro-genital sac Tocotrema,
{b) there are two gonotyls guarding the entrance to the
opening of the ventro-genital sac Rossicotrema,
111. The testes lie one behind the other ; the body is very
elongated Apophallus,
Tribe Heterophyea nov. tr.
Diagnosis : Heterophyinae in which the vitellaria do not extend
anteriorly beyond the level of the ovary.
Type genus : — Heterophyes Cobbold, 1866.
Genus Heterophyes Cobbold, 1866.
A. History of the Genus.
The genus Heterophyes Cobbold, 1866, is not only the first of the
family Heterophyidae, but is also one of the first genera to be formed
out of the mass of specific names of Trematoda, which were all
included in the generic name Distoma until the end of the last century.
It quickly attracted the attention of the investigators owing to a
peculiarity of the genital apparatus characterised by the presence
of a third so called ‘ genital sucker which distinguished it from all
hitherto known Trematoda,
Although the literature concerning this genus and its represen-
tatives is rather large, there exist few original works. Looss (1894
and 1902) provided descriptions of Egyptian species, and Japanese
authors (1915 and 1926) described two species from the Far East.
For the rest authors contented themselves with quotations or slight
modifications of the original descriptions.
The first species of the genus Heterophyes was Distoma heterophyes
Siebold, 1852, found in a man in Cairo during autopsy. This species
has been subsequently referred to by several authors under the
names : Distoma heterophyes hominis, Dicrocoelium heterophyes,
Fasciola heterophyes, Heterophyes aegyptiaca, Mesogonimus
heterophyes, Cenogonimus heterophyes, etc. In 1900 Stiles gave it as his
opinion that according to the international rules of nomenclature,
the correct name of this species should be Heterophyes heterophyes
(Sieb., 1852), as the genus Heterophyes Cobbold, 1866, had been
estabhshed with this species as type.
The early descriptions of this species were short and very
imperfect. The first attempt to give a detailed description with
figures was by Looss (1894 and 1896). Looss described two species —
Distoma heterophyes Sieb. from man, dog, cat, fox and Milvus
aegyptiuSy and a new species Distoma fraternum from dog, cat and
pelican.
Later (1902), Looss published a revision of the genus Heterophyes
in which he pointed out that in his earlier papers several species had
been described under one name. Looss reclassified his material on
a new basis and created six species and two sub-species out of the first
two species : (i) H. fraternus (Looss, 1894) sens. str. from pelican,
{2) H, inops Looss, 1902, from pelican and Milvus aegyptiusy
(3) H. aequalis Looss, 1902, from dog and cat, (4) H. dispar Looss,
1902, from dog and cat, (5) H, heterophyes (Sieb., 1852) from man,
dog and cat, (6) H, pallidus Looss, 1902, from Milvus aegyptiuSy
(7) H. heterophyes sentus Looss, 1902, from dog and cat, and
(8) H, dispar limatus Looss, 1902, from cats. The first four were
described in his first papers under the common name Distoma
fraternumy and the last four — under the common name Distoma
heterophyes.
At the end of Looss’s paper there is a note by Braun, adding
a ninth species to the genus Heterophyes y namely Cotylogonimus
persicus from a Persian wolf.
The genus Heterophyes was further enriched by two species from
the Far East — H. nocens Onji, 1915, and H, katsuradai Ozaki and
Azada, 1926. Thus, the number of species was raised to eleven.
However, in some recent works dealing with this genus the
opinion was expressed that some species may be invalid and that
their number should be reduced. In comparing the results of my
own studies with the literature, I carhe to the conclusion that only
three out of the described species may be considered as valid, namely :
1. H. heterophyes (Sieb.)
2. H, dispar Looss
3. H. aequalis Looss
146
H. nocens Onji requires further study to ascertain its validity,
and the following are certainly not valid :
(i) H, heterophyes sentus Looss synonym of H. heterophyes (Sieb.)
(2) H. Jraternus Looss „ „ „
(3) H. pallidus Looss „
(4) H, persicus (Braun) „
(5) H. inops Looss „ ,, aequalis Looss
(6) H, dispar limatus Looss „ „ dispar Looss
(7) H. katsuradai Ozaki and Azada... „ „ nocens Onji.
In my study I compared the data in the literature, particularly
the paper of Looss (1902), the most important of all, with the results
of investigations on my own material and some cotypes. Professor
J. Ciurea sent me a cotype of K, heterophyes obtained from Looss,
Dr. L. Szidat sent the type specimen of Coenogonimus persicus and
Dr. W. Arndt several bottles with Heterophyes species obtained from
Looss. Unfortunately, the specimens from the Berlin Museum proved
to be wrongly labelled and the collection could not, therefore, be
used as a standard.
Although I have not had all the types at my disposal, my studies
had this advantage, not enjoyed by other authors including Looss,
that I used not only material from naturally infected animals, but also
material from experimentally infected ones. Thus I had occasion
to investigate the development of features, which are the most
important for the differentiation of species, whereas to Looss there
were accessible some disconnected stages of these features.
I propose the following new descriptions of species since I con-
sider those of Looss to be based on an inevitably mistaken inter-
pretation of characters. The diagnosis of the genus Heterophyes
should also be re-defined.
B. Diagnosis of the Genus Heterophyes Cobbold.
Heterophyinae : Body tongue or pear-shaped ; the praepharynx
and oesophagus well marked ; the ventral sucker situated near the
middle of the body alongside the genital sac ; the testes are placed
slightly obliquely to the axis of the body ; the ovary hes on the
middle line in front of the testes ; the retort-like seminal receptacle
lies behind the ovary ; the vitellaria he behind the level of the ovary ;
the uterus winds between the testes and the ventral sucker ; the
seminal vesicle is divided into three parts separated from each
147
other by constrictions or short tubules ; the third part which is the
smallest and has thick walls is the expulsor ; the male and female
ducts unite before the genital aperture into a short ductus herma-
phroditicus which opens on the tip of the gonotyl ; the latter is a
protrusible body bordering on the ventral sucker on its left side and
behind it ; when erected it has the shape of a mushroom standing
on a wide and short leg ; at other times it is ring shaped ; the fret'
border of the gonotyl is armed with a circlet of spines, or comb-
shaped plates 25 to 87 in number, interrupted on the side adjacent
to the ventral sucker ; the excretory bladder is generally Y-shaped
with a short stem and branches ; it lies between the testes and the
seminal receptacle ; each branch receives a main vessel which is
formed at the level of the oesophagus by the union of several smaller
excretory ducts.
The adults parasitise the small intestines of mammals and birds.
The type species : — Heterophyeii heterophye^ (Siebold, 1852).
C. Life History of the Members of the Genus Heterophyes.
As has already been mentioned, one can at present distinguish
four species of this genus : H, heterophyes (Siebold), H. dispar Looss,
H, aequalis Looss, and H. nocens Onji, the latter being doubtful.
The life history of the representatives of the genus Heterophyes
has not yet been studied completely. Only a fragment is known,
namely the development of the metacercariae of H. heterophyes
in the dog, described by Khalil (1923) and that of //. nocens, described
by Onji and Noshio (1915).
According to these authors, the metacercariae both of the
Egyptian and Japanese species are located in the mirscles of fishes
of the genus Mugil, Infection occurs when dogs are fed on these
fishes. In short, the life history of the above species does not differ
from that of species of allied genera of Heterophyidae hitherto
described.
As the work of Onji and Noshio was not accessible to me and the
publication of Khalil bears the character of a short preliminary
report, I made a series of experiments in order to investigate the full
life history of the three species of the genus Heterophyes found in
Palestine. The dissections of the street dogs and cats in Jerusalem
showed that species of the genus Heterophyes are their most common
parasites. It was therefore concluded that their intermediate hosts
must be sought in fish sold in the market.
For the purpose of detecting which species of fish are carriers
of the larvae I obtained young dogs which had been taken away
from their mothers and brought up on milk and fed batches of these
animals with different species of fish. Several dogs were left for
control. After two weeks the dogs were sacrificed and examined.
It was determined that each of the following eight species of
lish, namely, Mugil cephalus, M. capito, M. anratus, Epinephelus
enaeus, Tilapia simonis, Lichia amia, L, glauca, and Barbus canus,
are carriers of all three species of metacercariae. — H. heterophyes,
//. dispar, diXid H. aequalis.
Encysted metacercariae were found without exception in every
specimen of mullet and usually in large number, irrespective of
the size or age of the fish. In one instance over one thousand cysts
were found in one gram of muscle of Mugil cephalus. In other
species of fish the metacercariae are rare, and one, therefore, may
conclude that the fishes of the genus Mugil are favourite hosts of the
members of the genus Heterophyes. The cysts are distributed
uniformly, chiefly in striped muscles, but also in heart muscle,
connective and fatty tissue, while they were not found in the skin,
gut walls, internal organs, fins, scales and gills.
I'he cysts of the three species of Heterophyes are so similar
morpliologically, that it is impossible to differentiate them. They
lie between the muscle fibres in the centre of a spindle-shaped mass
of fat globules (fig, i, c). The above formations are of different size,
a feature probably depending on age. There is no pigmentation of the
adhering tissue. The cyst itself, when examined through the lens on
a dark background, appears white. The cysts are round or slightly
oval and vary in size from o*i3-0’26 mm. Every cyst is isolated
from the surrounding fatty formation by a very thin homo-
genous membrane originating from the tissue of the host.
The wall of the cyst proper consists of a thick (0 004-0 01 2 mm.)
fragile shell and a thin inner membrane (0 001-0 002 mm.). The
shell breaks readily under the coverglass, and the metacercaria is then
delivered. On pressing the cyst the metacercaria often becomes
entangled in the inner membrane, and becomes free only after
further manipulation.
149
D. Morphology of the Metacercariae.
The metacercariae, like the cysts enclosing them, are very
similar in all three species. SUght differences are found in the siz^
and the internal anatomy. I shall confine myself to the description
of metacercariae of Heterophyes heterophyes , which is very typical.
Fk;. I. Metacercariae of 1! eterophyes heterophyes.
The metacercaria, enclosed in the cyst is folded on itself (fig. i, c)
and continually moves round the centre of the cyst. The anterior
part of the body is flattened, while the posterior one is round, and
appears to be distended by the large excretory vesicle, which in some
positions of the metacercaria occupies more than half of the cyst
and has the appearance of a dark sac filled with very small retractile
globules.
150
The larva, pressed out from the cyst is 0*21-0*40 mm. in length,
moves slowly and shows large changes in shape (fig. i, a, b). It lives
only for a few minutes. When fully stretched, it is tongue-shaped,
when fully contracted it is only half as long as in the retracted state
and is heart-shaped. The first three-fourths of the body are thickly
covered with scale-like spines. Numerous small masses of dark
])rownish pigment are scattered under the body surface.
Fig. 2. One day old Heteropbyes heterophyes from the dog.
In the living specimens one can make out only the suckers,
gonotyl, pharynx and excretory vesicle, while in stained prepara-
tions the early stages of the genital glands are also seen.
The oral sucker measures 0*03--0*05 mm. ; praepharynx, 0*015-
0*031 mm. ; pharynx, 0*028-0 031 mm. ; oesophagus, o*05-0*ii mm.
Just behind the bifurcation the intestinal caeca are twice as wide
as the oesophagus, but behind the ventral sucker they become much
narrower ; they reach the stem of the excretory vesicle. (In the
metacercaria of H. aequalis they extend only up to the testes.)
The excretory vesicle is heart-shaped and occupies almost one-
eighth of the body.
The ventral sucker is situated between the middle and the
posterior third of the body ; its diameter measures 0 03-0 04 mm.,
i.e., it is a little smaller than the oral sucker.
The gonotyl adheres to the left side of the posterior half of the
ventral sucker. It is always retracted and is about 0 02 mm. in
diameter. A horse-shoe shaped row of thickly arranged minute
spines is present in the middle of the gonotyl.
The immature testes are spherical, about 0-03 mm. in diameter,
being situated side by side in the posterior quarter of the body.
They are usually covered by the excretory vesicle. The ovary is
also spherical in shape, about 0.02 mm. in diameter and is situated
on the middle line a little in front of the testes.
E, Development of Hethrophyes in the Final Host.
By feeding dogs with fish containing metacercariae and sacrificing
some of them on successive days, one can easily follow the growtli
of the parasites and the development of their organs. It appears
that all three species of Heterophyes develop similarly. The features
peculiar to each species become evident during the first seven days.
Only the largest metacercariae which are probably the only ripe
ones develop into adults.
During the first two days after feeding, the anatomy of the young
trematodes does not differ markedly from that of the metacercariae
pressed out from cysts (fig 2). One day after the experimental feed
they are already absent from the stomach and are found between the
villi of the small intestine. Their posterior parts which are much
thicker than the anterior ones project beyond the surface of the villi.
It is not easy to detect them between the villi which they resemble in
size and colour. I have found them under the microscope in scrapings
of mucosa pressed between two glasses. The larvae are very motile
and change their shape by contraction and extension (fig. 3).
152
After the end of the second day, the larvae already reach
0-34-0-50 mm. in size. The excretory vesicle varies from Y-shaped
to heart-shaped, according to the amount of distension.
After the third day, the size of the body increases and there is
a marked development of the inner organs. The amount of pigment
decreases ; the testes, round or oval (0 06-0 08 mm.), often separated
from each other by the distended excretory vesicle, are seen
posteriorly ; in front of these the ovary is seen. The gonotyl
in many specimens becomes protruded — probably a .sign of the
beginning fertilisation. The vitellaria begin to form.
On the fifth day the trematode is up to o-8 mm. in length, the
tCvStes, o*o6~0’I2 mm. ; the ovary, o*04-o o9 mm. In almost 10 per
cent, of worms one or two transparent eggs are seen in the initial
portion of the uterus.
On the sixth day the length of the body is between o-8-i*i mm. ;
the testes, o*i mm. ; the ovary, 0'05-o*o8 mm. The vitellaria are
already well developed and the pigment has almost disappeared.
There are eggs in all specimens, their number varying from 2 to 50.
The majority of the eggs are still transparent, only the oldest being
yellowish.
On the eighth day some specimens reach 1-3 mm. in length. The
testes are o*io-o-i4 mm., the ovary o-07-oo8 mm. The whole
uterus is full of eggs which begin to escape ; at this stage they can
be detected in the faeces. The worms are more or less dark and are
long enough to project beyond the surface of mucosa. They can be
153
seen with the naked eye and appear as small dark dots studding
the surface of the mucosa.
I am not inclined to the view of Ciurea and Yokogawa, that young
Heterophyidae are confined to the villi of the mucosa only for the
first three days and afterwards escape into the lumen of the intestine.
They are confined to the villi in their early stages, but even as adults
the villi are their natural habitat. Their posterior ends project beyond
the surface of the mucosa because of their larger size. The oral
sucker is relatively smaller in adults than in the young stages and they
tend to fall out easily and are, therefore, found in the intestinal
contents.
Mature specimens are found mostly in the middle part of intestines
but they are sometimes found equally distributed throughout the
whole length of the small intestine.
F . Remarks on the Morphology of Adults.
Looss, and authors who followed him, relied on certain characters
to which they attributed specific significance, and on these characters
they distinguished nine species and two sub-species. A careful study
of hundreds of specimens belonging to three species, led me to the
conclusion that most of these features depend on age, on merely
individual peculiarities, or are due to fixation. The measurements
of the body which Looss determined very carefully are only of
relative importance. The living worms are very motile and, therefore
the shape and size of their bodies depend on the amount of contraction
at the moment of death. Worms which have been washed out from
the intestine and allowed to die in cold water have a constant shape
which does not change considerably on fixation in 70 per cent, alcohol.
Material which is fixed alive in alcohol or formalin contracts, more
so in formalin than in alcohol.
The dead worms found in the intestine of animals some time
after the death of the latter are almost always found to be extended.
The shape of the internal organs, which are elastic, depends on the
amount of contraction or extension of the worm (compare fig. 4 with
fig, 5b). The enumeration of the vitelline follicles is also of limited
importance for they vary in number and shape in every species.
These data were used by the previous authors because they were
considered of specific importance. Looss also considered the relation
154
between the sizes of suckers and the colour of eggs to be of great
specific importance. In spite of the fact that in his preface {1902)
he pointed out that the suckers grow with age, he gave very precise
measurements for every species, and further, he differentiated his
two subspecies (‘ formen ') — H. heterophyes sentus and H, dispar
limahis on this character.
A study of the developing worms show that Looss’s figures are
irrelevant. For, in the very young Heterophyes heterophyes the oral
sucker is the largest and the gonotyl is the smallest, while in the
adults the conditions may be reversed. This is seen from the Table II,
made from a series of specimens obtained from dogs.
'rABLE II.
Sliuwing the relall<»n between sizes of oral sucker, ventral sucker anti gonotyl of a series f)f
specimens of H . heterophyes from the dog.
l.cngLh of the worm
Oral sucker j
Ventral sucker
Gonotyl
Remarks
1
mm. 1
mm. 1
mm.
mm.
0-40
0*046
j 0*046
0*034
1 day old
0*6 1
0*046
0
6
0*068
3 days old
0-83
1 0*056
j 0*093
0*115
4 days old
0*94
1 0*065
0*133
0*152
6 days old
’ 0*074
1 0*229
i
0*232
24 days old
I 89
' 0*090
!
1 0*254
0*248
1-98
0*1 18
1 0*316
0*310
The colour of eggs to which Looss ascribed a great importance
is of no value for the differentiation of species. In every tube
containing wonns of the same age there are all gradations in the
colour of eggs, which vary from almost transparent to dark brown.
Specimens of Heterophyes heterophyes from Circaetus gallicus were
exceptional in that they had almost colourless eggs, like those of
Heterophyes pallidas Looss. It appears that the colour of the
eggs does not depend on the species of the worm, but on its environ-
ment.*
* Barlow (1925) made the same observation for the^ggs of Fasciqlopsis buski. This phenomenon
must have attracted the attention of all workers in the course of examination of faeces for eggs of
Trematodes and Nematodes.
Fig. 1. $ Anopheles culii
srapilisif PA0E«
OF Medical and Veterinary Importance.
156
membrane, which in parts is thickened by circular muscles. Also note the longi-
tudinal muscle bundle cut transversely ; these occur at intervals. This
section is through the dilated part of the mid intestine, which is usually known as
the stomach. There is little or no difference to be observed between the cells
lining the narrow part, the cardia, and those lining the stomach, except that
those of the latter are slightly longer. The circular fibres are well marked at
the lower end of the mid intestine, where they form a sphincter, which separates
the mid intestine from the hind intestine.
Class Hexapoda
Order Diptera
Suborder Cyclorrhapha
Family Muscidae Calypteratae
Subfamily Muscinae
Genus Musca.
Specimen 69. Entire alimentary tract of
$ Musca domestica, dissected out, fixed
to a coverslip with Bles*s fluid, stained
with Delafield’s haematoxylin, and
mounted in Canada balsam on a slide.
Fig. 95. Low power objective only.
As already noted, the alimentary tract in the higher Diptera is very long, and
there is no dilated flask-shaped portion as in the lower Diptera. It is thus a
more highly organized canal, and its increase in length and reduction in calibre
is of great advantage to these flies, as it has a much larger absorptive surface,
and the food is closer to the digestive cells. Fore Intestine. The fore intestine
of the house fly consists of the prestomum between the labella where the
pseudotracheal channels (collecting tubes, see fig. 205), lead into the food channel,
formed by the labrum-epipharynx and hypopharynx ; at the proximal end
it is continued on through the pre and midpharynx (buccal cavity), into the
pharynx, ph.y in the fulcrum, fu. It leaves it at the posterior end to become
continuous with the oesophagus, a., the first part of which is dilated, but soon
narrows and passes through the brain into the neck (see fig. 203, p. — - ) ; the
structure of the wall is similar to the oesophagus of Hcematopota, but is has more
muscular fibres. It passes into the thorax, ventral to the proventriculus, prv.^
which is a characteristic button-shaped structure, and is continuous with the
duct of the oesophageal diverticulum, so that the fluid food of the fly, as it is sucked
up into the fore intestine, passes straight on into the diverticulum. The oesophagus
communicates with the proventriculus by a short duct which passes upwards and
slightly backwards. (Esophageal Diverticulum, oe.dv. The oesophageal
diverticulum or crop, is a large thin walled sac, very similar to that of
Hcematopotay and is situated in the proximal part of the abdomen ventral to the
mid intestine. Its walls are much thicker than those of the corresponding
organ in the lower Diptera, the muscles and cells being distinctly more
conspicuous. It always contains the food which the fly has been feeding on,
and is commonly seen full of a yellowish fluid. Similarly, in the blood-sucking
Muscinse, the blood always passes into the oesophageal diverticulum, and later
is discharged into the mid intestine. This type of diverticulum is obviously
SyBC IMEIt PAGE.
156 Insects, Ticks, Mites and Venomous Animals
Fio. 96. Entire alimentary tract and salivary glands of $ Musca domestica. In such a dissection
it is not possible to demonstrate the normal relations of the oesophagus and proventriculus ; one
rectal papilla is shewn enlarged. /«., fulcrum ; hin.j hind intestine ; Ih.ep.^ labrum-epipharynx ;
labellum ; md.in., mid intestine ; Malpighian tube ; ce., oesophagus ; (B.dv,, oesophageal
diverticulum ; ph., pharynx ; prv,, proventriculus ; rc., rectum ; rc.pp., rectal papilla ; ph„
pharynx ; tJ., duct of one salivary gland ; salivary duct ; sl^., salivary gland ; tr., trachea ;
o., valve ; vtc., ventriculus.
155
G. Morphology and Classification of the Species of the
Genus Heterophyes,
Key to the Species. ^
A. T^ess than 30 rodlcts on the gonotyl :
(1) the intestinal caeca end at llic level of tlie
anterior part of the testes //. aequalis Looss
(2) the intestinal caeca extend beyond the posterior
borders of the testes H. dispar Looss
B. Not less than 60 rodlets on the gonotyl :
(1) not less than 62 rodlets on the gonotyl ; Near
East species 11 . hrtrrophyes {^\ch,)
(2) not more than 60 rodlets on the gonotyl ; Ear
East species //. iwccn.s Onji
Heierophyes heterophyes (Siebold, 1852).
(Figs. 1-9).
I found this species in the dog, cat, Palestinian fox and in
experimentally-fed rabbit and Circaetus gallicus. It is the largest of
the three species under consideration. The shape of the body in
non-con tract ed specimens depends on the host, being almost pear-
shaped in the dog and tongue-shaped in Circaetus gallicus and the cat.
The posterior part of the body is round or oval in cross section,
and is shghtly motile while the anterior part which is thinned
dorso-ventrally and convex dorsally, is very motile.
The size depends on the host, worms of the same age being
considerably smaller in the cat than in the dog.
The minimum size of a 7 days old specimen is o- 6 by 0-2 mm., the
maximum size is 2 7 x o cj mm. in the dog and 1*3 by 0 3 mm. in the
cat. The surface of the anterior two- thirds of the body is thickly
covered with rows of scale-like spines, arranged diagonally. The
spines are longest (up to 4//.) at the level of the pharynx and become
reduced in size posteriorly. The oral sucker is 0 05 -018 mm., the
ventral sucker o-o8-o*34mm. in diameter. They vary according to
the age of the worm. These variations are shown in 1 ‘ablc 11 . The
specimens from the cat have the ventral sucker comparatively a little
smaller than those from the dog (fig. 5). In young .specimens the
ventral sucker lies on the boundary between the middle and posterior
third of the body, in the adult it moves towards the middle of the
body.
157
The pharynx is oval, being 003-006 mm., the praepharynx
0 03-015 mm., oesophagus o o8~o-43 mm. in length. The intestinal
bifurcation lies on the boundary between the anterior and the middle
thirds of the body. The caeca are widest at the level of the ventral
sucker and are half as wide at the bifurcation and at the ends. They
reach the extremity of the body where they turn round behind the
testes. One caecum is often a little shorter than the other.
The testes are usually oval, but sometimes globular and are
situated in the extreme hind part of the body. They lie usually at
the same level, but the left testis is often situated a little anterior
to the right one. Their long axes are not parallel but form an angle
opening anteriorly. The right testis is usually somewhat larger
than the left one, their diameter varies between 0 05 mm. and
0 29 mm., according to size of the worm. The ovary is idways
globular in shape, 0 07-0- 15 mm. in diameter and lies in the middle
line in front of the testes. The testes and the ovary attain their
maximum size within the first two weeks, and therefore in large and
old specimens they appear relatively small.
A retort-shaped seminal receptacle, varying in size according to
the amount of distension with spermatozoa, lies behind the ovary.
The Mehlis' body (shell gland) is dorsal to the seminal receptacle.
The vitellaria consist of two bunches of irregular pear-shaped
follicles, scattered in the parenchyma under the ventral and lateral
surfaces of the body between the levels of the testes and ovary.
The vasa efferentia unite in front of the ovary and pass into two
seminal vesicles, separated from each other by a short duct. The
vesicles vary greatly in shape and size. The second seminal vesicle
is connected by a short tubule with a small oval or pyriform expulsor.
The ends of the male and female genital apparatus unite a short
distance before the genital aperture, which is situated on the tip
of the gonotyl. The gonotyl lies behind and on the left side of the
ventral sucker, and is usually protruded. It has the shape of a
mushroom and often overlaps a half of the ventral sucker (fig. 8).
In flattened preparations it has the shape of a round or oval disc.
The diameter varies between o-ii and 0-31 mm., depending on the
size of the worm and the degree of contraction. When protruded
it may be soinetimes larger than the ventral sucker, when retracted
it is usually slightly smaller. The border of the gonotyl is armed
•58
with a row of comb-shaped plates, interrupted only in the part in
contact with the ventral sucker. The number of the plates is 73-87,
their length 0 012 -0 018 mm. They lie in the derma and their 5-6
sharp dents project outwards. When the gonotyl is retracted, the
plates are also retracted and they then present the appearance of a
horse-shoe.
Fig. 6. llctcropbycs bctr/ophya from the dog, from a slightly distended specimen (flattened
preparation).
The uterus fills the whole free space between the testes and the
ventral sucker and does not extend beyond these levels. The eggs
are 0 023-0 027 mm. in length and 0 013-0 015 mm, in breadth ; they
159
may be transparent, or show various degrees of brown staining. Their
shell is thick and sometimes shows distinct ‘ shoulders.' The
measurements given by Looss — 0 030 by 0 0 17 mm. — must be
considered excessive.
6
Fig. 7. Longitudinal section through ventral sucker and gonotyl of Heterophyes heterophyet
showing : (tf) the gonotyl protruded ; (^) the gonotyl retracted.
I consider the following names as synonyms of Heterophyes
heterophyes : Heterophyes heterophyes sentus Looss, 1902, Heterophyes
pallidtis Looss, 1902, Heterophyes fraternus Looss, 1902 and
Heterophyes persicus (Braun) (other synonyms see in the reference
list of the bibliography).
H. heterophyes sentus was found by Looss in cats and differs from
the typical H. heterophyes in its somewhat smaller size and com-
paratively smaller ventral sucker. This resembles H. heterophyes
(Sieb.) which I have always obtained from experimental cats* As
dogs infected from the same material always contained typical
i6o
H. heterophyes, one must come to the conclusion that both species
are identical, though in the dog they reach a greater size than in the
cat.
Fifi. 8. N’entral sucker and protruded gonotyl of Heterophyes heterophves.
Heterophyes pallidus, from Milvus aegyptius, has been described
by Looss in his earlier works, as Distoma heterophyes Sieb. In his
paper of 1902, he created this species obviously on the principle that
similar species, parasitising birds and mammals, should be considered
as distinct. However, this principle cannot be applied to Hetero-
phyidae, since a considerable number of representatives of this family
are known to be able to parasitise both birds and mammals
[Apophallus miihlingi, Pygidiopsis genata, Monorchitrema taihui,
etc.).
Heterophyes pallidus, according to the original description, differs
from H. heterophyes only in having lighter eggs. The difference
between these two species is even less than between H, heterophyes
i6i
and H, heterophyes sentus. It is evident, therefore, that H, pallidus
is not a valid species and must be considered a synonym of H.
heterophyes.
I found this ' species,’ i.e., H. heterophyes with almost unstained
eggs in CArcaetus gallicus. This bird was caught young in the vicinity
of Jerusalem and hved in the laboratory for some months. It was
fed on meat, but occasionally fish [Mugil sp.) was given to it. As
no examination of its faeces was previously made, one cannot affirm
that it was infected with its trematode parasites in captivity.
However, the fact that H. heterophyes is found in CArcaetus gallicus,
confirms the view that H. pallidus Looss is a synonym of H. heterophyes
(Sieb.).
Among the material received from the Berlin Museum, there was a
tube labelled Heterophyes pallidus Looss, from Milvus aegyptius,
No. 4592. This sample proved to be typical Heterophyes heterophyes
(Sieb.)r Nevertheless, I cannot stress this as some of the tubes
of this same collection appeared to be evidently wrongly labelled.
I consider H. fraternus as a synonym of H. heterophyes. The
only description of this species is given in the paper of Looss published
in 1902. In his earlier works he described under this name two
different species — this and H. aequalis. The only drawing of this
species given in Looss’s work of 1896, apparently also represents
mixed features of these species, and, therefore, no conclusions can
be drawn from it. In any case, it does not correspond to the descrip-
tion given in 1902. In this description Looss pointed out that the
anterior and posterior halves of the body do not differ in width, while
on the drawing the body is distinctly pear-shaped ; according to the
description, the ventral sucker is considerably larger than the oral
sucker — on the drawing they are almost equal.
On comparing Looss 's description with my material of H eterophyes
heterophyes, it is impossible to find any difference between them. 1
have had no type specimens. The tube from the Berlin collection
labelled Heterophyes fraternus, No. 4591, proved to be identical with
Heterophyes dispar Looss.
I also consider H. persicus (Braun) to be a synonym of
H. heterophyes. I studied the type specimen of Braun kindly sent
to me by Dr. L. Szidat and found no difference from H. heterophyes.
It was an extended adult, measuring 2-54 mm. in length and
resembling in shape H. heterophyes as found in the dog. I also
investigated the cotype specimens of this ' species ' received from
the Berlin Museum (No. 3935) and found them to be identical with
the true H. heterophyes. They have been abnormally extended and
denuded of spines, a sign that their host died long before they were
removed from the intestine. The most extended specimens reached
3-8 mm. in length.*
1 'hus man, dog, Persian wolf, Palestinian fox, cat, rabbit.
Velecantis onocvotalus , Mihms aegyptius and Circaetus gallicus are all
hosts of H. heterophyes. The dog appears to be the most suitable
host, for the development of the parasite proceeds best in this animal.
It is probably the chief reservoir of H. heterophyes.
Heterophyes nocens Onji, 1915.
I retain H. nocens provisionally. Some authors (Lane, Leiper,
Faust) definitely consider it to be a synonym of Heterophyes
heterophyes. However, Ciurea does not agree with them but holds
it to be a valid species, and, still more, is of opinion that all Heterophyes
described from Japan as Heterophyes heterophyes should be considered
Heterophyes nocens.
On consulting the paper of Cort and Yokogawa, which contains
the only description of this species in a European language, I came
to the conclusion that the only feature that distinguishes this species
from Heterophyes heterophyes is the number of rodlets on the gonotyl
which in H. nocens does not exceed 60, but in H. heterophyes reaches
75-87. All the other characters mentioned by Cort and Yokogawa
are* unreliable for diagnostic purposes. Professor J. Ciurea has been
kind enough to send me a preparation of H. nocens, sent to him by
Professor Cort. Unfortunately I was not able to count the number of
rodlets on the gonotyl and I was not able to recognise any feature
that would distinguish it from H. heterophyes. According to its
general appearance, this specimen was markedly contracted (perhaps
during fixation). Therefore, the intestinal bifurcation was drawn
nearer to the ventral sucker whilst the gonotyl was retracted and
a little smaller than the ventral sucker. The eggs in the above
* In the same bottle I also found Heterophyes dispar Looss, H. aequalis Looss, Parascocotyle
hnga (Ransom), and Pygidiopsis genata Looss.
specimen measured 0 025 by 0*015, Uke those of Heterophyes
heterophyes, and not in accordance with the original description
(0-028 by 0 015).
The second Japanese species, Heterophyes katsuradai, recently
described by Ozaki and Azada, seems to be identical with H. nocens.
In distinguishing this species, the authors did not take into con-
sideration individual variations and the influence of fixation. Azada
pointed out inter alia, that the neck of JT. katsuradai with included
organs is much shorter than in other species of the same genus. The
author loses sight of the fact that his preparations had been fixed
in formalin and, therefore, it is not strange that they were strikingly
contracted. The vitellaria in H, katsuradai unite in front of the testes,
but they often do so in H, heterophyes. The eggs in H. katsuradai
are said to be smaller and darker than in other species — if compared
with my data, they are not smaller, and their colour is of no
importance.
Heterophyes dispar Looss, 1902.
(Figs. 9 and 10.)
I found this species in dogs, cats, and experimentally infected
rabbits, as well as in the sample of Trematoda received from tlie
Berlin Museum and labelled Cotylogonimus persicus from Persian
wolf. Its size is almost three-quarters that of H. heterophyes.
This difference became more evident on dealing with adult specimens
rather than with young ones. (It was easy to distinguish all three
species of Heterophyes in material obtained from experimental
animals infected by a single feed.) As in H, heterophyes, the worms
from cats are always smaller and more slender than those from dogs.
According to age and host, the length of this species varies between
0-4-I-4, the breadth o-2-0'4 mm. The specimens from the Persian
wolf were abnormally extended and reached up to 21 mm. in length.
The body is usually tongue-shaped or oval, the anterior part being
thinned with the lateral edges somewhat bent inwards. The posterior
part of the body is oval in cross section. Except for the posterior
extremity the whole surface is covered with large scale-like spines,
arranged in alternating rows. The spines are longest at the level
of the intestinal bifurcation, becoming gradually smaller towards
both ends and disappear entirely posteriorly. In young specimens
164
they are small and lie close to each other while in the adults they
are separated by greater intervals than in H. heterophyes.
In internal anatomy this species is very similar to H. heterophyes.
It differs mainly in the relative sizes of the ventral sucker and the
gonotyl and in the number of rodlets on the latter organ.
Fig. 9. Heterophyes dispar., adult specimen
from the dog.
Fig. 10. Young specimen of Heterophyes
dispar from the cat.
In adult specimens the oral sucker reaches 0 03-0 08 mm., the
ventral one o*o5-o-25 mm. in diameter ; the length of the praepharynx
is 001-006 mm., of pharynx 0 03-004 mm., of oesophagus
0 08-0. 12 mm. The intestine is sirnilar to that of H. heterophyes,
i.e,, the limbs arise from the oesophagus very wide and become twice
as thin behind the ventral sucker ; in the posterior end of the body
they bend behind the testes.
The globular or slightly oval testes are arranged almost side by
side in the posterior part of the body, the left one being sometimes
slightly in front of the other. The size of the left one is 0 04-0* 15 by
0 04-012 mm., of the right one 0*05-0*18 by 0 04-0*14 mm. The ovary
is round, 0 03-0*09 mm. in diameter. A small bean-shaped seminal
receptacle varying in size according to the degree of distension with
spermatozoa lies behind the ovary. The Mehlis' body hes usually to
the right of the ovary.
The vitellaria consist of two bunches of follicles of irregular
elongated pyriform shape, scattered in the lateral fields of the
parenchyma between the levels of the ovary and testes.
The termination of the male genital ducts is typical of the genus,
i.e., it consists of two seminal vesicles, separated from each other
by a short constriction and from the small expulsor by a short duct.
The uterus fills the whole free space between the testes and the
ventral sucker. Its end unites with the ductus ejaculatorius just
before the genital aperture to form a short common duct which opens
on the tip of the gonotyl. The latter adheres to the left side of the
hind part of the ventral sucker. Its diameter does not exceed half
that of the ventral sucker. Its border bears a row of thin spines,
25-30 in number, which is interrupted in the line of contact with the
ventral sucker. Each spine is provided with two or three minute
rodlets which are directed outwards.
The oval thick-shelled eggs are not distinctly narrowed at one
pole like those of H. heterophyes and they are usually stained brown.
Their size is 0*021-0*023 by 0 013-0 015 mm.
Heterophyes dispar appears to be the only species which has no
synonyms. I had Looss’s specimens of this species from the Berlin
Museum at my disposal (No. 4591 and No. 4615), but they were
wrongly labelled. Its hosts are dog, cat, Persian wolf and rabbit,
but it may, like H. heterophyes, subsequently be found to parasitise
other animals
i66
Heterophyes aequalis Looss, 1902.
(Fig. ii).
I found this species in dog and cat as well as in the material from
the Persian wolf. It is the smallest of the known species of the
genus ; its size being o*4-o*9 by 0-2-0-4 mm. The body is pear-
shaped or oval. The anterior part is somewhat flattened dorso-
ventrally, while the posterior one is round in cross section. Except
for the extreme hind part, the whole surface of the body is covered
with scale-hke spines, arranged thinly like those of H, dispar.
The oral sucker is 0 04-0-06 mm. in breadth, the ventral one
0 04-0-10 mm. Praepharynx 0 02-0 05 mm., pharynx 0 02-0 04
mm., oesophagus o-o6-o-ii mm. in length.
The intestinal limbs are four to five times as wide as the
oesophagus and their width is usually uniform. They reach the level
of the testes and never proceed beyond them.
The testes are nearly always globular and rather similar in size,
measuring 0 05-0-11 mm. in diameter. They lie almost side by side in
the posterior end of the body. When small they are separated by
the trunk of the excretory vesicle, when large they press against
each other.
The vasa efferentia open together into the hind seminal vesicle,
the latter is separated by a short constriction from the second seminal
vesicle which unites by a short tubule to the minute expulsor. The
short but elastic ductus ejaculatorius unites with the mouth of the
uterus to form a short common duct, opening on the tip of the gonotyl.
The ovary lies on the middle line somewhat in front of the testes.
It is globular, measuring 0-04-0-07 mm. in diameter. Behind it
lies a small bean-shaped seminal receptacle. The vitellaria consist
of about 10 to 16 large pear-shaped follicles, grouped radially round
the ovary. They seldom extend anteriorly beyond the front of this
organ or beyond the intestinal limbs.
The uterus fills the whole space between the testes and the ventral
sucker and opens into the common genital aperture.
The gonotyl is usually protruded and has the appearance of a disc
0 04-0-09 mm. in diameter, i.e., it is somewhat smaller than the
ventral sucker. Its border bears a circlet of 15 to 25 thin spines,
interrupted at the point of contact with the ventral sucker. The
16;
eggs are oval, 0 023-0 025 mm. long and o*oi4-o*oi6 mm. wide,
with thick shehs stained yellow or brown.
Looss also described Heterophyes inops from the pelican and
Milvus aegyptius in the paper in which he described H. equalis.
In comparing these two descriptions one is forced to the conclusion
that they refer to one and the same species ; 25 to 35 spines on the
gonotyl, caeca extending up to the anterior part of the testes, are
their common and very characteristic features. All the remaining
Fig. 11. Heterophyes aequalisy from the dog.
differences such as the size of the body, of the suckers, etc., indicates
rather the age or the degree of contraction of the worm, but cannot
be considered as specific characters.
It is evident that there are no anatomical differences between
H. aequalis and H. inops but only difference in host such as exist
between H, heterophyes and H. pallidUs, Probably here, too, Looss
distinguished these two species because one parasitises birds, and
the second mammals. Thus there is no doubt that H. aequalis and
H. inops refer to one and the same species. The question arises.
i68
which of the two names is valid. I think that H. aequalis should
be retained because under this name Looss described the parasites
of carnivora, which are their main hosts, for in them they develop
best.
The dog, cat, Persian wolf, pelican and Milvus aegyptius should
be considered as hosts of H. aequalis.
In a tube from the Berlin collection, labelled No. 4614, there were
three specimens of this species from a cat from Cairo. Their sizes
are o*34-o*49 by o-iy-o iS mm. However, the glass No. 4615 labelled
' Heterophyes inops Looss, Felis dom. Cairo ' proved to contain
specimens of H. dispar Looss. (The label is obviously wrong because
Looss recorded ‘ H. inops ' only from the pelican and Milvus aegyptius,
but not from the cat.)
H . Occurrence of Heterophyes Species.
After feeding dogs and cats with suitable fish I invariably found
all the three above-described species of Heterophyes. Under natural
conditions these species do not occur with equal frequency. In
dogs in Jerusalem Heterophyes heterophyes is found in 70 per cent.,
H. dispar in 40 per cent., H. aequalis in 20 per cent., while in cats
respectively 80 per cent., 40 per cent., and 30 per cent. Cats are thus
infected more frequently than dogs. This is explained by the fact
that refuse bins are more accessible to cats than to dogs.
In all cases of the occurrence of the representatives of the genus
Heterophyes in the above mentioned animals H. heterophyes is always
found to predominate, H. dispar never occurs alone, but only as
accompanying the former, and in numbers not exceeding 5 per cent.
H* aequalis again does not occur alone, but only in the presence
of two former species, not exceeding i per cent, of the number of
H. heterophyes. This correlation was found both in dogs and cats
in experimental and in natural infections. All three species occur
together only in heavy infections. The number of worms found in
natural infections varies from a few to several, thousands. In an
experimental dog, fed several times with mullet, I counted over 13,000
specimens of these parasites.
There is only scanty information as to the occurrence of H.
heterophyes and the Japanese species in man. The former has been
found several times in Egypt, while the eggs of the latter are common
169
in men (over 18 per cent.), in some districts of Japan. In Jaffa and
Jerusalem the ova of Heterophyes are often found in faeces of man,
examined in the laboratories of the Hadassah Medical Organisation.
However, one must accept this date with reserve because other
Heterophyidae such as Dexogoninms, Monorchitrema , etc., possess
eggs which are similar to those of Heterophyes and can easily be
mistaken for them. These remarks apply particularly to Palestine,
where fourteen species of Heterophyidae occur.
Below, descriptions of other Palestinian Heterophyidae are
given. Some of them have already been described by otlier authors
but my researches revealed some differences (often considerable)
from the existing descriptions It is probably due to the mode
of investigation and particularly to the method of fixation of the
material. The following descriptions are based on tlie investigation
partly of living material and partly of mounted preparations of
specimens which were allowed to die in water and directly fixed
in 70 per cent, alcohol. For elucidation of morphological details,
serial sections were made.
The life-history of each species is not given, for in all cases it
resembles that of Heterophyes heterophyes. In all species the life-
cycle of which has been studied experimentally, the mtdacercariae
are similar in appearance ; they are encysted in the muscles of
fishes and the adults begin to lay eggs on the eighth day after the
infecting feed.
Genus Metagonimus Katsurada, 1912.
Up to the present three species of the genus Metagonimus have
been described : M. yokogawai (Katsurada, 1912), M. romanicus
(Ciurea, 1915 ), and M. dohrogiensis (Ciurea, 1915 ). Some authors
presume that all these species are identical. I suggest that the
two latter species are identical, for their original descriptions offer
no sufficient grounds for separating them ; the specific name
M. romanicus should be retained for them.
According to the original descriptions there exist some small
differences in the structure of the ventro-genital sac of M. romanicus
and M, yokogawai. It is probable that these species arc identical,
but further comparative study is necessary before this point can
be settled.
170
Genus Dexiogonimus n. gen.
This genus is closely related to the genus Metagonimus Katsurada
from which it differs only in the position of the testes. The
difference between these two genera might be compared to that
between other genera of Heterophyidae, as for instance, Apophallus
and Rossicotrema,
Diagnosis : Heterophyinae. — ^Body rounded posteriorly, tapered
anteriorly, anterior part may be slightly wider than the
posterior one ; praepharynx and oesophagus well marked ; the
ventral sucker is modified, having a tubule-like slit instead of
a cavity and is included in the ventro-genital sac ; the testes
lie side by side at the posterior extremity of the body ; the large
globular seminal receptacle lies in front of the right testis ; the
ovary lies in front of the testes on the middle line ; the retort-like
seminal vesicle may be divided by constrictions into several parts ;
there is no expulsor ; the vitellaria are situated behind the level
of the ovary ; the uterine coils fill the free space between the levels
of the testes and the ventro-genital sac and do not extend beyond
these organs ; the ventro-genital sac is situated near the border
of the body, its opening being guarded by small muscular papillae ;
the excretory vesicle is Y-shaped with the stem as short as the
branches. The adults are parasites of birds and mammals.
Type species : — Z). ciureanus n. sp.
Dexiogonimus ciureanus n. sp.
(Figs. 12-17).
This specific name is given in honour of Professor J. Ciurea, who
has made valuable contributions to the knowledge of the
Heterophyidae,
Dexiogonimus ciureanus is frequently found in Palestinian dogs
and cats, particularly in the neighbourhood of Lake Tiberias, where
it is very common. I also found two specimens in an undetermined
Larus sp. from the same locality. The second intermediate hosts
are : Tilapia simonis, T, galilea, Barbus canus, Discognathus sp.,
Mugil cephalus, M, capito, Lichia glauca, the first two being the
main ones.
The body of normal specimens has a peculiar typical shape
somewhat resembling the sole of a foot, narrow posteriorly and
wide anteriorly. The anterior and posterior parts are separated
by a shght constriction. The specimens fixed alive in formalin,
e.g., very contracted, are almost pentagonal. The specimens from
Larus sp. were pear-shaped and were remarkable for their small size.
As this fish-eating bird harboured only two specimens of
Dexiogonimus one may suppose that it is not a suitable host and
that the Trematodes found were young specimens which would
have been shortly passed out.
The length of the body is 0'7-i-3 mm., the maximal breadth
0-3-0 *7 mm. The whole body, except the hindmost part, is thickly
covered with spines, which are longest at the level of the intestinal
bifurcation. The oral sucker is 0 05-0* 09 mm. wide, the prae-
pharynx 0*02-0* 06 mm., the pharynx o* 03-0* 05 mm., and the
oesophagus 0*06-0*09 mm. long.
The intestinal bifurcation is situated on the boundary between
the first and second fourth of the body. The caeca are three times
as wide as the oesophagus. From the bifurcation they pass obliquely
towards the margins of the body, the right one turns in front of the
ventro-ge^iital sac, the left one some distance behind it, i.e., they
are asymmetrical. They both reach the level of the middle of the
testes.
The testes he at the hind border of the body. They are globular
or oval with the long axis horizontal, 0*09-0*18 mm. in diameter.
When small they are separated by the stem of the secretory vesicle,
when large they are adjacent.
The ovary is globular, o* 07-0 *13 mm. in diameter, and lies
on the middle hne in front of the testes, from which it is separated
by some uterine coils. To the right and a little behind it lies the
seminal receptacle, which varies in size, according to the amount of
distension by spermatozoa. When fully distended it may be larger
than the ovary.
The vitellaria are situated at the margins of the body between
the levels of the testes and the ovary! They consist of 15 to 30 small
irregular follicles on each side.
The uterus in ripe specimens fills the whole free space between
the level of the testes and the genital aperture. Some distance
172
before the genital aperture it unites with the ejaculatory duct to
form a hermaphroditic duct.
The vasa efferentia open into a voluminous seminal vesicle
0 3 mm. in length, variable in shape and often showing two or
three constrictions. An ejaculatory duct arises from the seminal
vesicle and unites it with the uterus.
Fig. 12. Dexiogonimus ciureanus from the
dog, from a preparation fixed in alcohol.
Fig. 13. Dexiogonimus ciureanus from the same
host as that of Fig. 12, after fixation in formalin.
There is no expulsor. The prostatic cells form a mass at the
junction of the male and female ducts. The hermaphroditic duct
formed by this junction opens on the median wall of the ventro-
genital sac. The latter is situated near the right border of the
body at the level of the junction of its first and middle third. It is
an elongated depression directed s(Mnewhat obliquely to the axis
173
of the body and occupied by a large oval muscular body which is
a modified ventral sucker. The latter may be completely retracted
into the sac or its apex may protrude for a «?hort distance.
Fig. 14. Longitudinal section through the vcntro-genital sac of Dexiogonimus ciureanus (semi-
diagrammatic).
An oval transversely muscular papilla projects from the median
border of the ventro-genital sac closing its aperture. Another
muscular papilla is present on the dorsal wall of the sac just behind
the former. The genital aperture lies behind the dorsal papilla —
a condition which appears similar to that found in Metagonimus
yokogawai. Both papillae together may be considered as a peculiarly
modified gonotyl.
The eggs are oval with the anterior pole somewhat narrower
than the posterior, their length is o o 25 -o -028 mm., their width
0*015
Genus Diorchitrema n. gen.
Diagnosis : Heterophyinae — Body pear-shaped, the praepharynx
and oesophagus well-marked ; globular ventral sucker included in
the genital sac ; the testes lie side by side at the posterior extremity
of the body ; the ovary in front of the right testis ; the globular
seminal receptacle in front of the left testis ; the single small seminal
vesicle is connected with a large expulsor ; the vitellaria confined
174
behind the level of the ovary ; the uterine coils do not pass beyond
the levels of the testes and ventro-genital sac. The ventro-genital
sac is situated near the middle line and contains no gonolyl. Adults
are parasites of mammals.
Type species : — Z). pseudocirrata n. sp.
Diorchitrema pseudocirrata n. sp.
(Fig. 15).
The representatives of this species are rare parasites of dogs
and cats in Palestine. Their second intermediate hosts are fishes
of the genus MugiL They are small worms, reaching o-3-o*6 mm.
in length and 0-2--0-3 mm. in breadth. The body is almost round
in cross section, the anterior portion being narrower than the posterior
one. The whole body, except the most posterior part, is covered
with small spines.
The oval sucker is o-04-o-o5 mm. in diameter; the praepharynx
is 001-0 04 mm., the pharynx 0*03-0 04 mm., the oesophagus
0*07-0 *14 mm. in length. The intestinal bifurcation is situated in
front of the middle of the body ; the intestinal caeca are equal,
some times thicker than the oesophagus and reach the anterior
borders of the testes.
The testes lie at the same level at the posterior border of the body.
They are globular or slightly elongated and measure 0 06-0*12 mm. in
diameter. When they are small they are separated from each other
by the stem of Y-shaped excretory vesicle, but usually they are
large and adjacent.
The globular ovary, 0 03-0*05 mm. in diameter, lies in front of
the tfestes to the right of the middle line. To the left and a little
behind it lies the seminal receptacle, which, according to the amount
of distension, may be larger or smaller than the ovary.
The vitellaria consist of 20 to 40 large elongated follicles dispersed
between the dorsal surface of the body and the testes.
The vasa efferentia open into a small, usually globular seminal
vesicle, 0*018-0*037 mm. in diameter, connected by a short tubule
with the expulsor. The latter is oval and relatively very large,
being 0 07-0* 10 mm. long and 0*04-0*06 mm. wide, with very thick
walls in which spiral fibres are clearly seen. It lies in the middle
I7S
portion of the body at the left side and is obhque to the long axis
of the body. A short ejaculatory duct arises from the expulsor
and unites with the end portion of the uterus. The junction of the
uterus and ejaculatory duct is surrounded by a mass of prostatic
cells.
Fig. 15. Diorchitrema pseudocirrata^ from the dog.
The uterus in adult specimens fills the whole free space between
the expulsor and testes. It joins the ejaculatory duct to form
a short hermaphroditic duct opening into the genital aperture.
The latter opens on the dorsal wall of the ventro-genital sac at the
base of the small ventral sucker, 0 03-0 04 mm. in diameter. The
ventro-genital sac lies to the left of the middle of the body.
The eggs are oval, 0 018-0*021 nim. in length and 0*009-0*012 in
width.
176
Gemis Stictodora Loess, 1899
This genus was created by Looss for the species S. sawakinensis
Looss, 1899 found in a sea-gull. Owing to the imperfect interpretation
of the structure of the terminal portion of the male duct this genus
could not be included in any group of Trematodes and for this
reason Poche created for it a special family — Stictodoridae.
Examination of a cotype received from the Berlin Museum
(No. 4594) and the material obtained from Palestinian animals
both infected naturally and experimentally proved its relation to
the Heterophyinae.
The diagnosis of the genus Stictodora may be modified as
follows : Body elongated ; both praepharynx and oesophagus well
marked ; ventral sucker absent ; the testes lie in the middle of the
hind part of the body obhquely to its axis, the ovary in front of
the right testis, the globular seminal receptacle between the testes ;
the seminal vesicle consists of two parts divided by a constriction ;
it unites with a small expulsor. The vitellaria are confined to the
posterior third of the body ; the uterus coils between the genital
aperture and the posterior extremity of the body ; the genital sac is
filled by a large protrusible gonotyl armed with spine-hke plates ;
the genital aperture opens at the base of the gonotyl ; the excretory
duct is Y-shaped with the stem as short as the branches. Adults
parasitise mammals and birds.
Type species : — 5 , sawakinensis Looss, 1899.
Stictodora sawakinensis Looss, 1899.
(Figs. 16-18).
Looss found this species in a Lams sp. and referred it to the
family Monostomidae, In his description he reported the presence
of a cirrus pouch, containing a small pars prostatica, ejaculatory
duct and .a thick armed (spinous) cirrus. Looss mistook the
peculiarly constructed ventro-genital sac of this Trematode for the
cirrus pouch.
Stictodora sawakinensis is found rarely in dogs and cats in
Palestine and always in small numbers. I found it once in a bird —
Puffinus kuhli, brought from Suez. The specimens of Stictodora
177
sawakinensis from the bird were considerably smaller than those
from mammals.
The second intermediary host of 5. sawakinensis in Palestine are
fishes of the genus Mugil.
Body oblong, in normal state of distension and divided by
a slight constriction into two parts — a short and narrow anterior one
and a longer and wider posterior one.
Fig. 1 6 . Stictodora sawakinensis, from the dog.
Fig. 17. Stictodora sawakinensis, from Puffinus kuhli.
Fig. 18. The gonotyl of Stictodora sawakinensis in the state of erection.
The anterior part is flat and concave like a spoon, while the
posterior one is oval in cross section. The very contracted specimens
are pear-shaped, with both extremities rounded, distended specimens
are tongue-shaped.
178
The length of the body is o-6-i'4 mm., the maximum width
o*2-0'4 mm. The oral sucker is 0 05-0 07 mm. in diameter, the
praepharynx 0 04-0 09 mm., the pharynx o*04-o o6 mm., the
oesophagus o- 04-0 08 mm. in length.
The intestinal bifurcation in contracted specimens lies on the
boundary between the first and second fourths of the body. The
caeca are as wide as the oesophagus, straight, and reach almost to
the posterior extremity of the body.
All the reproductive organs except the vitellaria are grouped
in the third fourth of the body. The testes are round or trans-
versely oval, o- 06-0 10 mm. in cross section and lie at an angle to
the middle line, the left one in front of the right one. Between
them lies an almost round seminal receptacle of varying width.
The ovary is round, 0 05-0 08 mm. in diameter and lies, in normal
specimens, in front of the right testis, but in stretched out specimens
it lies between the testes while the seminal receptacle is pressed
behind the left testis.
The vitellaria consist of rather small follicles arranged in trans-
verse rows in the hind fourth of the body ; the largest follicles lie near
the border, the smallest near the middle line.
The vasa efferentia open into a large elongated and curved
first seminal vesicle, which lies in front of the left testis. This
vesicle is connected with a second smaller one, which is united by
a short duct to a small expulsor from which the ejaculatory duct
arises.
The uterus after leaving the seminal receptacle proceeds by
a winding course towards the hind extremity of the body along the
right side, turns forward, passes to the left testis, proceeds between
it and the seminal receptacle and reaches the genital aperture.
A little before its termination it may dilate up to 0-07 mm. in width
to form a small egg receptacle usually filled with eggs.
The male and female ducts open side by side on the median wall
of the genital sac.
In total preparation the genital sac has the appearance of a ring
0 04-0 07 mm. in diameter lying on the right side and a little in
front of the middle of the body. The whole vplume is occupied
by a pear-shaped gonotyl which has a globular base and a cone-
shaped retractile appendage. When contracted, the appendage is
179
totally withdrawn into the globular base, when extended it protrudes
above the surface of the body in the form of an angular cone covered
with six to ten longitudinal rows of triangular plates, 0 015 mm. long.
There is no ventral sucker either in the genital sac or outside it.
The eggs practically fill the whole posterior quarter of the body
and are oval in sliape with thick shells stained dark brown. I'heir
length is 0*027-0 030 mm., the breadth 0 015-0 017 mm.
The excretory vesicle is Y-shaped, its branches being as long as
the stem. The right branch is adjacent to the right testis.
(ienus Galaclosomtim Looss, i8qq.
1 'wo species may be assigned to this genus, G. erinacetmi (Poirier,
1886) and G. lacteum (Jagerskjold, 1896). Both are insufficiently
described and it is not unlikely that when their descriptions will be
complete they will hnd another position in the sub-family. As far
as may be concluded from their actual descriptions, the genus
Galactosomuni is closely related to Stictodora and differs from it
mainly in the structure of the (‘xcretory bladder which is S-shaped
and not Y-shaped.
(jeiius MicrolisirKfn Braun, 1901.
riiis genus was created by Braun to include three species :
M. cochleae (Diesing, 1850), M, cochlear if or me (Rudolphi, 1819) and
G, spinelum Braun, 1901. Braun has misinterpreted tlie structure
of the copulatory apparatus of these species, and this was corrected
by Odhner (1910). The latter author pointed out the similarity of the
genus Microlistrum Braun, with Galactosomum Looss, and expressed
a suj^position that these two genera may be idcnticed. Meanwhile,
these two genera must remain separated because of differences in the
arrangement of tlie genital glands.
According to jagerskjold (1908), ;l fourth species may be added
to this genus, Monostomum semifuscum Olsson, 1876. However, as
the original description is insufficient and the types of this species
are lost, a re-description of new material from the same host — Sula
basana — is necessary to verify this point.
i8o
Tribe Cryptocotylea ii. tr.
Diagnosis : Hetevophyinae, in which the vitellaria extend
anteriorly up to the level of the genital pore or beyond it.
Type genus ; — Cryptocotyle Liihe, 1899.
Although the earlier authors have distinguished the sub-families
Cryptocotylinae (Liihe, 1899), Tocotreminae (Looss, 1899), ApophalUnae
(Ciurea, 1924), which partly correspond to the tribe Cryptocotylea,
the latter could not hitherto be created as incorrect criteria have
been used for classification.
The above sub-families were based on the details of the ventro-
genital sac, while in fact characters of higher rank only must be used
for making a sub-family. 'I'he creation of a sub-family for this
group of Heterophyidae seems, however, to be previous. Tliis step
may be justified later, when many still undescribed forms will be
revealed.
Genus Cryptocotyle Liihe, 1899.
TJie genus Cryptocotyle , 1899, was made almost at the same time
as the genus Tocotrema Looss, 1899. Since the type species of
both these genera are characterised by similarly constructed ventro-
genital sacs, i.c\, by similar characters used for generic identification,
file name Tocotrema was suppressed in favour of Cryptocotyle by
all later writers.
According to my experience, the structure of the ventro-genital
sac may unite into one genus only species in which other essential
characters are similar. In the species designated as types for
Cryptocotyle and Tocotrema essential differences exist in the arrange-
ment of the testes and in the shape of the body, both these characters
being correlated. I'hus, these two species cannot be retained in
one genus but must be separated, i.c., both Cryptocotyle and Tocotrema
should be considered valid.
Vhe diagnosis of the genus Cryptocotyle may be modified as
follows : —
Heterophyinae. Body almost round or pentagonal, praepharynx
short ; oesophagus well developed ; the rudimentary ventral
sucker is included in the ventro-genital sac ; the testes lie side by
side at the posterior margin of the body ; the ovary in front of the
right -testis* ; the seminal receptacle in front of the testes on the
middle line ; the seminal vesicle (?) ; the vitellaria extend anteriorly
beyond the level of the genital pore ; the uterus coils between the
levels of the ovary and ventro-genital sac ; the latter is situated
near the middle of the body ; the excretory vesicle Y- or T-shaped,
with short stem and branches. Adults parasitise mammals and
birds.
Type species : — C. concavum (Creplin, 1825).
In addition to the type species two more species should be
included in this genus — C. quinqueangulare (Skrjabin, 1923) and
C. cryptocoiyloides (Issaitschikolf, 1923). Both these species have
been originally described under the generic name Ciureana Skrjabin,
1923. The above genus was thought to differ from Crypiocotylc
only in having bean-shaped eggs, a feature more marked in
( . quinqucangtdare than in C. cryptocoiyloides, 'J'his feature must,
however, be considered as not more than specific and therefore
I consider the creation of the genus Ciureana to be unjustified.
1'he existing three species of the genus Crypiocotylc may be
determined according to the following key :
A. Testes lobed or serrated :
(0 C' (Crejdin, 1K25)
(2) eggs bcaii-sliaped C. cryptocotyloidrs
(Issaitschikoff, 1923)
B. 1 estes not lobed (/. quinqueangulare
(Skrjabin, 1923)
1 had no representative of this genus in my collection and can
therefore add no details concerning them.
(ienus Tocoirema (Looss, 1899).
Diagnosis : Heierophyinae. — The body elongated, oval or tongue-
shaped ; the praepharynx and oesophagus vary in length ; the
testes lie in the hind extremity of the body, obliquely to its
axis ; the seminal receptacle in front of the right axis ; the ovary
in front of the seminal receptacle ; the seminal vesicle long and
coiled, passes into an elongated expulsor ; the vitellaria may reach
•Several authors described the ovary as situated in other places but these assertions arc
probably erroneous.
i 82
anteriurly up to the intestinal bifurcation ; the uterine coils lie
between the level of the ovary and the genital aperture ; the ventro-
genital sac is situated on the middle line of the body, contains
a conical gonotyl and on the dorsal wall a depression which may be
regarded as a rudiment of the ventral sucker (?) ; the excretory
vesicle is approximately Y-shaped, but the stem is long and curved
like an S, while the right branch is somewhat shorter than the left one.
Adults parasitic in mammals and birds.
Type species : — T. lingua (Creplin, 1825).
Three species should be referred to the genus Tocotrema ; T. lingua
(Creplin, 1825), T. jejunum Nicoll, 1907, and T. echinata (Linstow,
1878), but I was not able to assure myself of the validity of the
last two. I have not had the material for comparison but the
specimens of T. jejunum kindly sent to me by Professor Ciurea
may be equally diagnosed as T. lingua.
The validity of T. echinatum is problematical, as the original
description is very inadequate. Liihe (1909) regarded it as belonging
to the genus Cryptocotyle, but as ifs testes are arranged obliquely
it cannot remain in that genus. Ciurea (1924) maintains that the
specimens in America are distinct from the type and proposes for
them a new name — Cryptocotyle americanum. As a justification
for this emendation he records some insignificant differences from
T. lingua, which may be due to the method of fixation, but are
certainly not of specific importance. Further comparative study
should clear up this confusion.
(ienus Rvssicolrema Skrjabin, 1919.
The genus Rossicotremci was created by Skrjabin with R. dvniciim
Skrjabin, 1919, as type. Ransom (1920), without taking into account
the work of Skrjabin, published his new genus Cotylophallus with
two species — C. similis and C. venustus. As Ciurea pointed out,
these two genera are identical and the name Rossicoirema should be
retained as valid.
A study of the cotype specimens of Apophallus brevis Ransom,
1920, kindly sent me by Professor J. Ciurea, showed that this species
must also be regarded as a member of the genus Rossicoirema.
Thus, four species should be attributed to the above genus,
183
R. donicum Skrjabin, R. simile (Ransom), R. vemisium (Ransom),
and R. breve (Ransom). The detailed comparison of data in the
literature shows, however, that the most essential differences
between the species mentioned are only in the thickness and dis-
tension of the vitellaria follicles. This feature cannot, of course,
be acknowledged as important enough to decide on the validity
of species, and therefore I hold all the above-mentioned specific
names as synonyms of Rossicotremu donicum Skrjabin, 1919.
The diagnosis of the genus Rossicotrema should be modified as
follows ; —
Heterophyinac. Body oval, narrower anteriorly than posteriorly ;
the praepharynx short, oesophagus long ; ventral sucker included
in the ventro-genital sac ; the testes lie at the posterior extremity
of the body obliquely to its axis ; the seminal receptacle lies in
front of the right testis ; the ovary in front of the seminal recep-
tacle ; the seminal vesicle is composed of several (two or three) parts
separated by constriction ; the vitellaria extend anteriorly almost
up to the intestinal bifurcation ; the ventro-genital sac is situated
on the middle line of the body and contains two small gonotyls arising
at the sides of the genital aperture ; the excretory vesicle is Y-shaped
with an S-like bent stem. The adults are parasitic in mammals and
birds.
Type species : — R. donicum Skrjabin, 1919.
Genus Apophallus I.iihe, 1909.
Three species of this genus liave been hitherto described :
A, muhlingi (Jagerskjold 1899), A, brevis Ransom, 1920, and.d. major
Szidat, 1924. As previously shown, A. brevis is a synonym of
Rossicotrema donicum Skrjabin. A. major is a synonym of
A. muhlingi, the size is the only difference between them. This
feature depends on the age of the worms and cannot be regarded
as a character of specific importance. The findings of Ciurea (1924)
confirm this supposition : this writer found specimens of A . miihlingi
smaller than the type specimens and larger than the specimens
described by Dr. Szidat. Professor Ciurea and Dr. Szidat kindly
sent me their specimens and I was thus able to recognise the identity
of these two species.
184
Among the specimens sent by Dr. Szidat there was one from
a cat. It is the first record of a natural infection with A. miihlingi
in a cat. This specimen is very small, and it is probable that cats
are not suitable hosts for A . miihlingi.
The diagnosis of the genus Apophallus should be modified as
follows :
Heterophyinae. Body very elongated ; praepharynx sliort,
oesopliagus long ; the globular ventral sucker is included in the
ventro-genital sac ; the testes lie almost one behind the other in the
posterior extremity of the body ; in front of them lie the seminal
receptacle and the ovary ; the seminal vesicle is long and coiled
and may be divided into several parts by constrictions ; the
vitellaria extend from The posterior extremity of the body up to the
level of the genital opening or still farther anteriorly ; the uterine
coils lie between the levels of the ovary and genital pore ; the
ventro-genital sac is situated on the middle line ; in addition to the
ventral sucker it contains two tubercle-like gonotyls guarding the
genital pore ; tlie excretory vesicle fias a long S-like bent stem and
short branches. Adults parasitise mammals and birds.
1 'ype specimen: — A. miihlingi (Jagerskjold, 1899).
Sub-family Centrocestinae Looss, 1899.
Diagnosis : Heterophyidae. — The body rounded posteriorly,
tapering anteriorly ; oral aperture surrounded by more or less con-
spicuous spines ; the oral sucker has, in some genera, an anterior
lip-shaped appendage and a caudal conical appendage ; two testes
situated posteriorly to other reproductive organs.
Type genus : — CentrocesUis Looss, 1899.
This sub-family contains at present five genera which, similarly
to Heterophyinae, might be divided into two tribes, i.e., according
to the degree of development of the vitellaria. The number of
genera is, however, too small to make the division necessary. The
following is a key to the genera : —
A. The vitellaria do not extend anteriorly beyond the level
of the ovary :
(1) the caudal appendage of the oral sucker absent ...Pygidiapsis EoosSy
(2) the caudal appendage of the oral sucker present ...Parascocotyle Stunkard
and Haviland, 1924*
B. The vitellaria reach anteriorly up to the level of the
genital aperture :
(1) the caudal appendage of the oral sucker absent . ..Centrocestusl^oo^t, 1899,
Staninosoma Tanabe,
1922
(2) ihc caudal appendage of the oral sucker present ...Ascocotyle TiOoss, 1899
. It is seen that the genera ('entrocestiiS and Stamnosoma are not
separated in this key. In fact the differences between them are so
slight that they may be regarded as identical. If one compares
the discussion of Faust and Nisliigori (1926) on the validity of the
genus Stamnosoma, and the diagnosis of Stamnosoma cited by Stiles
and Hassall (1926) with the original description of C entrocesiiis , the
conclusion is reached that the differences between these two genera
are not of generic rank. I leave, however, the genus Stamnosoma
since I was not able to examine the types or original descriptions.
I had only the representatives of the genus Pygidiopsis and
Parascocotyle at my disposal.
Genus Pygidiopsis Looss, 1907.
Diagnosis : Centrocestinae. — The pear-shaped body divided into
an almost globular posterior part and a concave anterior part ; the
oral sucker has no appendages ; praepharynx long, oesophagus
short ; the ventral sucker is included in the genital sac ; the testes
lie at the posterior margin of the body, side by side ; the seminal
vesicle, in front of the testes on the middle line ; the ovary, ventrally
to the seminal receptacle ; the seminal vesicle may be divided in
parts by constrictions ; the vitellaria are situated at sides of the
testes ; the uterus coils between the levels of the ovary and the genital
sac ; the ventro-genital sac is situated on the middle line and contains
a small gonotyl in its left anterior angle ; the excretory vesicle is
T-shaped with the branch equal to the stem. The adults parasitise
mammals and birds.
Type species : — P. genaia Looss, 1907.
Pygidiopsis genaia Looss, 1907.
(Fig. 22).
This species was found by Looss (1902) in the pelican in Egypt,
by Ciurea (1924) in Rumania, in the dog by Faust in China and
by Linton (1928) in the United States in Butorides virescens (see
Ascocoiyle plana). I found this species among the Trematodes sent
from the Berlin Museum (host, Persian wolf).
In Palestine this species is a rare parasite of dogs and cats. The
second intermediate hosts in Palestine are Tilapia galilea, T. nilotica,
T. simonis and Barbus cams.
Tic. 22. Pygidiopsis genataj from the dog.
The body consists of an almost globular posterior part and a
flattened anterior one. Normally the worm is bent ventrally with
the anterior part concave ; when flattened it is pear-shaped or
triangular. The length of mature wonns is o-4~o-7 mm., the
breadth 0-2-0-4 mm. Except for the hind portion the whole body
is covered with thick scale-like spines. Round the oral aperture
there is a row of spines, i6 in number, which are twice as long as those
of the integument and are only seen on fresh liiaterial.
The oral sucker is oval or globular, 0 03-0 05 mm. wide and does
not possess a funnel-like appendage. The praepharynx is
0-03-O I0 mm. long, and when contracted shows a bulb-like dilation
posteriorly. The pharynx is 0 02-0 04 mm. long. The oesophagus
is short — 0 03-0 06 mill. I'he caeca reach the level of the ovary
and there turn somewhat dorsomedially.
The testes are round or transversely oval, 0 06-014 mm. in
diameter. They lie side by side in the posterior extremity of tlie
body. A large globular seminal receptacle, o ()7-o i4 mm. wide
lies immediately in front of the testes on the middle line of the body
near its dorsal surface. A globular ovary 0 04- 0 08 mm. in diameter
lies a little to the right and ventrally to the seminal receptacle,
'fwo seminal receptacles of varying sizes, separated from each oth(‘r
by a constriction, which may disappear on distension by spermatozoa,
are situated on the left side of the body, in front of the seminal
receptacle, one behind the other. The second vesicle is connected
by an ejaculatory duct with the terminal portion of the uterus.
The vitellaria are situated at the angles of the posterior extremity
of the body and consist each of five to eight large pressed follicles
arranged in single longitudinal rows. The uterus fills the free space
between tlie testes and the ventro-genital sac and opens in the left
angle of its anterior wall.
The ventro-genital sac is situated at the middle of tlie body and is
occupied by a globular ventral suck(;r 0 04 0 06 mm. in diameter.
In the left angle of the ventro-genital sac near the genital aperture
there is a small oval gonotyl, the so-called ‘ lenticular-shaped body ’
0 04-0 06 mm. in the long axis. In some cases the ventral sucker
may partly protrude from the sac but the gonotyl is always covered
by the dorsal border of the latter.
The eggs are oval, 0*018-0 022 mm. long and 0 009-0*012 mm.
wide and are provided with a conspicuous filament on the posterior
pole.
Genus Parascocotyh Stunkard, 1924.
Up to the present five distinct species of this genus have been
described. They have all been attributed by the earlier authors
to the genus Ascocotyle Looss. Stunkard and Haviland (1924) defined
the generic peculiarities of Ascocotyle and showed that the type
specimen of this genus A . coleostoma (Looss) differs so markedly from
other allied species that it appeared necessary to separate it from
them. They therefore created the genus Par ascocotyle for the
remaining species.
In the genus Ascocotyle there are two roWvS of circumoral spines
and several coils of the uterus wind in front of the genital aperture,
while in the genus Parascocoiyle there is only one row of circumoral
spines and the coils of the uterus confine themselves behind the
genital aperture. Another essential difference between these two
genera, which Stunkard and Haviland did not point out, is the position
of the vitellaria, which in Ascocotyle extend in front of the ventral
sucker, while in Parascocoiyle they do not pass anteriorly beyond the
level of the ovary.
It should, however, be pointed out that, while the distinction
(){ the genus Parascocoiyle by Stunkard and Haviland is fully justified,
the creation of the species Parascocoiyle diminnla by these authors
appears to be iinnece.ssary. I consider P. diminnla as a synonym
of P. mimita (I.ooss), for the differences on which this species was
established can be attributed to age or fixation and are not of specific
value.
Ciurea (1924) stated that in species encountered in America the
ventral sucker is included in the genital sinus, while in others it
lies on the ventral surface of the body, and on this basis all the species
might be divided into two genera. I'his view is based on a mis-
interpretation of the position of the ventral sucker, which has been
wrongly described by previous authors as lying above the ventral
surface of the body. Probably in all species of Parascocoiyle the
ventral sucker is included in the genital sac, at least in the majority
of them, as I have had occasion to observe.
Diagnosis : Centrocestinae. — Body pyriform ; the dorsal wall
of the oral sucker is provided with a contractile triangular lip-like
appendage anteriorly and with a conical appendage posteriorly ;
the oral aperture is surrounded by a single row of conspicuous spines ;
praepharynx long, oesophagus short ; the ventral sucker is included
in the genital sac ; the testes lie side by side at the posterior margin
of the body ; the seminal receptacle in front of them on the middle
line, the ovary in front of the right testis ; the seminal vesicle is
divided in parts by constrictions ; there is no marked expulsor ;
the vitellaria are situated at the sides of the testes ; the uterus coils
between the testes and the genital opening ; the ventro-genital
sac is situated on the middle line and contains besides the globular
or oval ventral sucker, one or two tubercle-like gonotyls, the surface
189
of which may bear chitinized bars ; the excretory bladder is Y- or
T shaped. Adults parasitise mammals and birds.
Type species : P. minuta Looss, 1899.
The following is a key to all known species of the genus
Paraficocotyle, including a new species P, ascolonga . P.pithecQphagicola
(Faust, 1920), which is included in this key, is insufficiently described
and requires further study for justifying its systematic position or
even validity.
A 'Fhc caeca reacli only up 10 ilic level of ihe ventral sucker :
(1) adeejuately des^crlhed species P. mhiula (Looss)
(2) insuflicienily descri[>ed species P. pithecaphnoicolu
(Faust)
JL q'hc caeca reach the ovary or more posteriorly ;
(1) tlic vilellaria compact :
(<?) the appendix of the oral sucker readies the
pharynx P. nsrojojioa n. sp.
{b) the appendix of the oral sucker half as lont^ as tlie
praepharynx P. itulicn
(Allessand rini)
(2) vilellaria divided into follicles :
(ri) the uterine coils entangled ; one muscular
papilla in front of the genital aperture P. luina (Ransom)
(/>) the uterine coils have a transverse direction ; there
arc two muscular papillae in front of the
genital aperture P, longa (Ransom)
Parascocotyle longa (Ransom, 1920).
(Figs. 23 and 24).
This species which has hitherto been reported only from the
Alaskan fox was frequently observed in Palestinian dogs and cats.
I also found this species among other Heterophyidae in a bottle
labelled * Cotylogonimus persicus from the Persian Wolf. (No. 3935)/
Braun, who examined this material, evidently overlooked specimens
of P. hnga.
In dogs the worms occur mainly in the hindgut.
The secondary hosts in Palestine are Mugil cephalus, M. capito,
Lichia amia, Barbus canis.
Parascocotyle longa is the largest species of the genus, the length
reaching 0*5-1 2 mm., the width o*3-o*4 mm. Normally the worms
190
are pear-shaped, elongated and concave ventrally. ITie body, except
the posterior extremity, is covered with minute scale-like spines.
The oral sucker has the appearance of a beaker 0 05--0 06 mm.
wide with a funnel-like appendage (but not an empty sac, as thought
by some authors). The praepharynx is o- 14-0*37 mm. long, passes
Fig. 23. Parascacoiyle longa^ from the dog.
ventrally to the caudal appendage of the oral sucker and reaches
up to the end of the first third of the body, while the appendage
extends for not more than two-thirds of this distance. The appendage
is generally bent like an S and is apparently non-contractile ;
however, its configuration may vary in different specimens
(compare figs. 23 and 24).
The oral sucker is surrounded by a single row of 16 large spines,
18-20/X long. The dorsal border of the oral sucker projects
as a triangular lip which is not apparent on contraction. The
pharynx is 0 05-0 07 mm. long. The oe.sophagus is short and is not
seen in very contracted specimens. The caeca reach up to the testes ;
their ends bend slightly dorso-medially.
I'lG. 24. 'I'he oral sucker ol PuuiACocotylr lotij'dj ^\ilh a contracted lip and bent posterior appendage.
I'he testes, o o6'O i2 mm. in diameter, arc round or oval trans-
versely. riiey lie side by side at the posterior extremity of the body
and when large they are contiguous. The globular ovary is
0 04-0 08 mm. in diameter, and lies in front of the right testis and
some distance from it.
The large globular seminal receptacle lies on the middle line of
the body just in front of the testes. A small Mehlis' body is situated
behind the seminal receptacle. The vitellaria are situated laterally
to the testes. They consist of five to eight large globular follicles
arranged in single rows. The second follicle (counted backwards)
is always very wide and extends internally beyond the others.
The vasa efferentia open into the large seminal vesicle, which
is 3 -shaped or consists of two vesicles separated from each other
by a constriction. The seminal vesicle lies in the left side of the body
midway between the seminal receptacle and the ventro-genital sac.
From the upper part of the seminal vesicle an ejaculatory duct arises
which unites with the terminal portion of the uterus just before the
genital opening.
The uterus fills the whole free space between the level of the ovary
and the genital opening. It makes five to eight transverse ^oils
which pass from side to side of the body, and open on the dorsal wall
of the ventro-genital sac. The latter is situated in the middle of the
body in the centre of a conspicuous elevation. The sac is filled
by the rudimentary oblong ventral-sucker, 0 04-0 06 mm. in diameter,
usually directed obliquely. In the anterior wall of the sac there is
a transverse slit, in the middle of which the genital opening is situated.
On each side of the genital opening there is a depression filled by
a tubercle-like gonotyl o oa-o-oq mm. wide, of irregular shape. The
gonotyls bear on their surface nine to twelve minute chitinous bars.
The eggs are typical for the genus, i.c., they are small, 0 018 by
o 09 mm., almost transparent, with a thin shell and flat operculum.
Parascocvtyle ilalica (Alessandrnii, 1906).
(Fig. 25).
Four specimens of this species were found on one occasion in a
dog in Jerusalem together with some specimens of Parascocotyle
ascolonga and numerous specimens of Parascocotyle longa.
The worms are pear-shaped, 0.7-0.8 mm. long and 0‘2-o-^ mm.
wide. Except the hindmost portion of the body the whole surface
is covered with small scale-like spines.
The oral sucker 0 06 mm. in diameter is beaker-shaped ; its dorsal
wall bears a triangular retractile lip, which may disappear on con-
traction, and behind a funnel-like appendage ending at the level
of the middle of the oesophagus. The praepharynx is 0 09-010 mm.,
pharynx 0 05 mm. and oesophagus 0 03-0-04 mm. long.
The caeca are two to three times as wide as the oesophagus and
reach the level of tlie ovary where they bend slightly dorso-medially.
193
The testes are globular, 0 08 mm. wide, and lie side by side in the
hindmost portion of the body. A large seminal receptacle lies ip
front of them in the middle line. The globular ovary 0 05-0*06 mm.
in diameter lies on the right and a little in front of the seminal
receptacle. The vitellaria arc two solid masses of irregular outline
lying along the lateral borders in the last quarter of tlie body.
I'lG. 25. Parascocotylc italica, from the dog.
ThP coils of the uterus fill the whole free space behind the genital
aperture. The vasa efferentia open into one of two large transversely
oval united seminal vesicles situated between the seminal receptacle
and the genital aperture.
194
The latter opens on the dorsal wall of the ventro-genital sac,
between the base of the globular ventral sucker (o o5--o-o6 mm. in
diameter) and a small oval gonotyl. The oval eggs (0 019 mm.
long, 0*009-0 010 mm. wide), are narrowed at the anterior pole, and
have a thin shell.
This species closely resembles P. nana (Ransom). The only
essential ditference between these two species lies in the arrangement
of the vitellaria. In P. italica the latter form solid masses while in
nana they are divided into follicles. I ascertained this difference
on comparing my specimens with cotypes of P, nana, kindly sent
me by Professor M. C. Hall.
Parascocotyle ascolonga n. sp.
(Figs. 26-28).
1 found this species in dogs and cats, usually in 'small numbers.
Experimentally it was obtained by feeding dogs with Tilapia simonis,
and T, galilea.
The body is o*5-o-7 mm. long, is spindle- or pear-shaped with the
maximum breadth in the posterior extremity (o* 1-0*3 mm. broad).
Except the hindmost part, the whole body is covered with sriiall
scale-like spines.
The oral sucker has the .shape of a beaker o*()4-o*07 mm. wide,
bearing in front a retractile triangular lip and provided beneath with
a long funnel-.shaped solid appendix which reaches the anterior margin
of the pharynx, and in contracted specimens may extend even beyond
this. The oral aperture is surrounded by a single row of 16 large
spines 0 018-0 022 mm. long. The praepharynx is 0*04-0*15 rnin.,
pharynx 0*02-0 04 nim., oesophagus 0*009-0 018 mm. long.
The intestinal caeca are of equal width and reach the level of the
seminal receptcicle, where they turn somewhat dorso-ventrally.
The testes, 0*04-0*10 mm. in diameter are usually globular and lie
side by side in the hind extremity of the body ; occasionally they are
contiguous. A large seminal receptacle, the size of which depends
on the amount of distension with spermatozoa lies in front of the
testes on the middle line. The globular or transversely oval ovary,
0 02-0 06 mm. long and 0 06-0 07 ^ 5 ^* wide, lies a little in front and
to the right of the seminal receptacle. The vitellaria appear as two
elongated masses lying along the border of the hind extremity of the
body ; anteriorly they reach the level of the ovary.
The vasa efferentia open into one of the two voluminous seminal
vesicles which lie midway between the seminal receptacle and the
ventro-genital sac. The ejaculatory duct, which arises from the
second seminal vesicle, opens into the terminal portion of the uterus
just before the genital aperture.
Fig. 26. Parascocotylc ascolonga, from the dog.
The tangled coils of the uterus fill the whole free space between
the genital aperture and the testes and often extend behind the latter.
The genital sac lies almost in the middle of the body. It is filled
196
by a round ventral sucker 0 04-0 05 mm. in diameter. On the left
side of the anterior wall of the ventro-genital sac there is a slit at the
bottom of which is situated a small tubercle bearing the genital
aperture. Between it and the aperture of the slit lies a small oval
gonotyl 0 02-0 03 mm. in long axis. This slit is contractile and when
contracted, the gonotyl may be extruded.
Tig. 27. I'he contracted anterior extremity Fig. 28. Longitudinal section through the
• of Purascoiotylc ascolonga. anterior portion of Parascocotylc ascolonga
(scmi-diagramraatic).
The eggs are 0 018 mm. long, 0 009 mm. wide, with thin shells,
somewhat narrowed anteriorly and with distinctly visible opercula.
This species resembles P, nana (Ransom) on the one side and
P. iialica (Aless.) on the other. It differs from the first in the length
of the appendix of the oral sucker, which always reaches up to the
pharynx, independently of the amount of contraction or distension,
but not up to the n;iiddle of the praepharynx, and in the arrangement
of the vitellaria which are compact, masses, and not divided into
follicles. , .
197
From P, iialica (Aless.) it differs only in the character of the
appendix of the oral sucker. I separated the latter two species
only because I found no intermediate conditions in the specimens
examined. In the four specimens of P. iialica the appendix of the
oral sucker was uniformly short while in all the specimens of
P. ascolonga examined this appendix was found to reach the pharynx.
I assume that the funnel-like appendix of the oral sucker in the
representative of the genus Parascocoiyle may change its position,
but does not contract to any extent, and therefore its relative length
may serve as a specific character.
Sub-Family Cercarioidinae n. subf.
Diagnosis : Heterophyidae with flattened and markedly dilated
anterior part of the body, without circumoral spines, with two testes
situated behind the ovary.
Type genus : Cercarioidcs n. gen.
Besides the type genus this family also contains the genus
Scaphanocephalus Jagerskjold, 1903. The differences between these
two genera are shown in the following table : —
Cercarioidcs
Scaphanoccphalus
Shape of the dilation
Inverted heart
Irregular with lolded edges
Oral sucker
Large
i
Small
Position of the testes
1
Removed from the posterior j
extremity of the body
In the posterior extremity of the
body
Position and extent of the
vitellaria
Posteriorly to the anterior
testis
Up to the intestinal bifurcation
Genus Cercarioidcs n. gen.
Diagnosis : Cercarioidinae. — Body elongated, divided into two
distinctly separated parts : the anterior one flat heart-shaped and the
posterior one spindle-shaped, oval in cross-section. Praepharynx
198
and oesophagus very short. The testes lie in the middle of the
posterior part of the body one behind the other. In front of them
in the order named lie the ovary and the seminal vesicle. The
vitellaria are scattered in the posterior part of the body, posteriorly
to the ovary. The uterus fills the whole open space in the posterior
part of the body. The ventro-genital sac lies in the middle of the
constriction dividing the body.
Type species : — C. aharonii n. sp.
Cercurioides aharonii n. sp.
(Fig. 29).
I found only one specimen of this species in Paffinus knhli, caught
near Suez. Its name is given in honour of Mr. J. Aharoni, the
indefatigable ecologist of Palestine to wliom I am indebted for the
determination of the definite and intermediate hosts cited in this
paper.
The length of the whole body if 3 4 mm. The first third of the
body is flattened and is heart-shaped with the base posterior. It
is connected with the posterior spindle-shaped part of the body
by a narrow constriction. The relation between the lengths of these
two parts is I : 2. The anterior part is covered witli long and thin
spines, while the first half of the posterior part with much shorter
but thicker spines. The end of the body is free from spines.
The large oral sucker 0-38 mm. in diameter is situated ventrally
on the anterior extremity. It is followed by the pharynx 014 mm.
in diameter, which passes immediately into the intestine. The
caeca first pass obliquely forward before reaching half-way to the
edges of the body, turn towards the constriction and then become
somewhat narrowed. They pass along the sides of the body up to
0-43 mm. from its posterior extremity.
The ventral sucker is probably included in a small ventro-
genital sac, which is 0 05 mm. in diameter and lies on the middle
of the constriction between the two parts of the body.
The slightly lobed testes lie in the middle third of the body.
The posterior testis, 0 38 mm. in diameter lies near the right caecum.
The ovary is globular, 018 mm. in diameter and lies near the right
caecum, tnidway between the anterior testis and the ventro-genital
sac. Immediately behind it lies the Mehlis* body.
The vitellaria consist of many large follicles of irregular shape
199
scattered throughout the whole posterior part of the body, behind
the ovary.
The vasa efferentia flow into a wide vas deferens which opens
into an oval first seminal vesicle measuring 015 by 0 09 mm. The
latter opens into the second small seminal vesicle 0 04 mm. wide.
Both vesicles lie between the ovary and the ventro-genital sac.
Fig. 29. Cfrcarioides aharoniiy from Puffinus kuhli.
The coiled uterus fills the whole free space of the posterior part
of the body. The genital aperture was not well seen in the only
mounted specimen, but seems to open into the ventro-genital sac.
The course of the excretory bladder was not determined. The eggs
are oval, 0 037 mm. long and 0.022 mm. wide.
200
Sub-family Haplorchinae (Looss, 1899) Poche, 1926.
This sub-family was created by Looss, under the incorrect name
Haplorchiinae to contain the genera Haplorchis and Galactosomum.
In the present paper the latter genus is assigned to the Heterophyinae
and the genus Monorchitrema is included into the Haplorchinae,
This sub-family is very near to the Heterophyinae and might be
united with it but for the different number of testes.
Diagnosis : Heterophyidae with flattened but not dilated anterior
part of the body ; circumoral spines absent ; one testis ; the ovary
and seminal receptacle situated in front of the testis.
Type genus : — Haplorchis Looss, 1899.
Genus Haplorchis Looss, 1899.
I had no representatives of the genus Haplorchis at my disposal
and therefore cannot have a clear view of its peculiarities, for it is
highly probable that in 1899 Looss did not use the most essential
characters for classification. I include this genus as the published
figures of its members bear a close resemblance to the genus
Monorchitrema, which belongs to the Heterophyidae. It is, however,
highly possible that after the revision of the type-specimens these
genera will prove identical and the genus Monorchitrema will fall
into synonymy.
Two species of the genus Haplorchis are known : H. cahirintis
(Looss, 1896) and H. pumilio (Looss, 1896). It is noteworthy that
the first is the only species of Heterophyidae found in the adult stage
as a parasite of fish. This circumstance leads to the supposition
that H. cahirinus may belong to quit€ another family.
Genus Monorchitrema Nishigori, 1924.
Diagnosis : Haplorchinae. — Body oval or elongated ; praepharynx
absent, oesophagus long ; ventral sucker absent ; the testes lie
at the posterior extremity of the body, the ovary in front of it ;
seminal receptacle near the right border of the body ; the seminal
vesicle consists of several parts ; an expulsor may be present ; the
vitellaria lie in the posterior part of the body behind the level of the
ovary ; the uterus coils at the sides of the testis and in front of it ;
the genital sac is situated on the right side of the middle line and
201
contains a large gonotyl which bears on its surface chitinous rodlets
or other armature ; the excretory vesicle is Y-shaped. The adults
parasitise mammals and birds.
Type species : — A/, taihokni Nishigori, 1924.
MoiiorchUrema taihokui Nishigori, 1924.
(Fig. 19).
This species was discovered in Formosa as a parasite of a bird
Nycticorax nycticorax. l^xperimen tally it has been obtained by Faust
and Nishigori in man, dog, cat and in small laboratory animals.
'I'he first intermediate host in Formosa ])roved to be a fresh-water
snail Melania reiniana var. hidachiens, the second — 12 species of
fish of the families Cyprinidae, Sikiridae and Colitidae.
In Palestine this species is a rather rare parasite of dogs and
cats and is seldom present in large numbers. I found it on one
occasion together with M onorchitrema taihui and Dexiogonimns
cmreanus in a Lams sp, caught near Lake Tiberias. I have obtained
it experimentally in dogs and cats by feeding them with Barbtis
canus, Barbus longiceps, Tilapia simonis, T. galilea, T, niloiica, Mugil
capito.
It is probable that this species is a synonym of Haplorchis pumilio
(Looss) but I have not had the possibility of determining this point.
Although Faust and Nishigori (1926) gave a detailed description
of this worm, I give it below again, for some details require further
elucidation.
The worms are elongated and have rounded extremities. The
posterior part of the body is round in cross section, the anterior part
is somewhat flattened. The length of the body is o ^-o-y mm., the
maximum breadth o i-o-3 The whole surface of the body
is covered with small scale-like spines. The oral sucker is
0 04-0 05 mm. in diameter ; the praepharynx is short, almost
disappears on contraction and when distended reaches 0 03 mm. in
length ; the pharynx is 0 02-0 04 mm., the oesophagus 0 08-014 mm.
long ; the intestinal bifurcation situated between the first and middle
thirds of the body ; the caeca are three to four times as thick as the
oesophagus, they narrow somewhat towards their ends and reach
the boundary between the middle and the last third of the body.
202
The single large globular or long-oval testis is 0 07-0*12 by
0 05-0*10 mm. in diameter and lies in the hind part of the, body ; just
in front of it lies the globular ovary 0 03-0 06 mm. in diameter.
To the right of the ovary lies the seminal receptacle, which varies in
size. To the left and somewhat in front of the seminal receptacle
)ie two seminal vesicles separated from each other by a short neck.
The first is fairly small, the second large. The large vesicle
is connected with a small expulsor and the latter gives rise to a short
ejaculatory duct which unite with the end portion of the uterus.
* Fig. 19. Afonorrhitrrma taihokui^ from the dog.
The vitellaria are scattered under the dorsal surface of the body
and consist of two united groups of large elongated follicles, 16 to 20
in number.
The uterus passes from the ovary to the left, bends round the
testis, turns forward and after a sinuous course reaches the genital
aperture, which opens in the median wall of the genital sac. The
latter is situated dextrally to the middle of the body. It is occupied
by a semi-circular gonotyl, which protrudes partly from the opening
of the sac. This protruding part 6 t the genotyl forms the true
203
posterior and lateral border of the opening of the genital sac and
bears on its surface a row of about 40 very minute spines. At the
bottom of the sac there is a depression paved with large cells, clearly
visible in total preparations as a darkly stained spot, which is
apparently a rudiment of the ventral sucker.
The eggs are 0 028-0-032 mm. long and 0 014-0 018 mm. wide,
they often possess a minute filament on the posterior pole.
MonoYchilyema taihui Nishigori , J q 2 ^ .
(Figs. 20 and 21).
This species was found in F'ormosa together with the one described
above by feeding man and experimental animals with seven species
of fish belonging to the famiUes Cyprinidae , Siluridae and Colitidae,
The first interrnediate host of this sj^ecies in Formosa is a snail Melania
ohlique-granosa (Smith) .
In Palestine, mainly in the vicinity of the Lake Tiberias this
species is not uncommon in dogs and cats. I found a few species
on one occasion in Laras sp. near I.ake 1 'iberias. 'flie worms were
smaller than those from carnivora.
Flxperimentally I obtained it after feeding dogs with fish :
V aricorhinm sp., Tilapia simonis, Barbus cams and Ganihusia
affinis. In the latter species the metacercariae were found in the
muscles, under the skin, in the fins and tail, while in others only
in muscle.
This species is much larger than the previous one. They both
frequently occur together but they can easily be distinguished by
their sizes.
The length of the body is 0*5-1 2 mm., the maximum breadth
o*24“0*4 mm. The normally distended specimens are elongated
in shape, with the anterior part flattened and the posterior one oval
in cross section. The contracted specimens are oval in shape.
Almost the whole body is covered with small spines which are longest
on the first third of the body, becoming smaller towards the posterior
extremity.
The oral sucker is 0 05-0 07 mm. in diameter. Praepharynx is
seen only in very distended specimens in which it does not exceed
0.018 mm. ; pharynx 0 02-0 05 mm. in length. The long oesophagus,
0 II-0-28 mm., is somewhat dilated posteriorly and reaches the
204
boundary between the first and the middle third of the body. The
caeca are three to four times as wide as the oesophagus and reach
the posterior extremity of the body.
There is only, one very large testis, o* 12-0-21 mm. in diameter,
filling, in some specimens, the whole space of the posterior quarter
of the body. It is round or oval with the long axis longitudinal.
Fig. 20. Monorebitrema taibui, from the cat.
In front of the testis lies a globular ovary o- 05 -o-it mm. in diameter.
To the right of the ovary lies the seminal receptacle which may be
smaller or larger than the ovary.
The vasa efferentia open into the first small seminal vesicle which
is separated by a constriction from second and larger oiie. From the
205
latter a short ejaculatory duct emerges and opens into the uterus
some distance before the genital aperture.
The uterus proceeds from the ovary to the left, bends along the
border of the testis, proceeds to the end of the left caecum, turns
back, bends round the testis up to the end of the riglit caecum turns
back, and finally proceeds to the genital aperture. Its Terminal
portion may be distended, forming a small egg-receptacl(\
Fifj. 21. Lonj^ltudinal section through the vcntro-genital sac of Monorchitrema talhiti.
The genital sac is situated to the left of the middle of the body
and is ring-shaped (o o8“O i2 mm. diameter). It is occupied by a
large gonotyl, which, owing to a slit in its median border, is almost
semi-circular. The surface of the gonotyl is peculiarly ornamented
by 14 to 18 chitinous bars 0 014-0 028 mm. long, arranged like a
fan. On the hind median angle of the gonotyl there are again four
to six conspicuous spines directed backwards. Dorsally to the
gonotyl, in the bottom of the genital sac there is a depression paved
with a layer of flat cells, which is apparently the rudiment of the
ventral sucker.
The genital aperture opens on the median wall of the genital
sac opposite to the slit of the gonotyl.
The eggs are oval, 0 025-0 028 mm. long, 0 012-0 015 mm. wide.
206
wSub-FaMILY ADLERIINAE NOV, SITBF.
Diagnosis : Very small Heierophyidae with oval or spindle-shaped
body round throughout its whole length, without circumoral spines,
with a single testis situated anteriorly to the ovary and the seminal
receptacle.
Type ^QX\\\s \ -Adleria n. gen.
Cienus Adleria n. gen.
This generic name is dedicated to Dr. vS. Adler through whose
efforts the Helminthological Laboratory was established in the
Hebrew University.
The diagnosis of this genus coincides with the diagnosis of the
sub-family, As seen from the latter the anatomical structure of
Adleria is an aberrant one when compared with other genera of
Heierophyidae. I placed this genus among Heterophyidae because
of the presence of a seminal receptacle^ a seminal vesicle and a gonotyl.
Adleria niinntissima n. sp.
(l''igs. 30-33)-
This very interesting trematode is found rather rarely in
Palestinian dogs and cats, usually in small numbers. I obtained
large quantities of these worms by feeding dogs with fishes :
Discognathus sp., V aricorhinns , sp. Barbus canis, Mugil cephaltis,
M. capito.
The parasites are distributed throughout the whole length of the
intestine of its host, but are most numerous in the first parts. They
penetrate deeply into the villi and can be washed out only after
their death. They remain alive for some fifteen minutes in scrapings
of the intestinal mucosa where they are motile and change their
shape as shown in fig. 33. They live only for one to two minutes
in water.
These trematodes are very small, their length being o* 27-0 47 mm.
their breadth 0 09-015 mm. The body is pear-shaped or spindle-
shaped, round in cross section throughout its whole length. It is
covered with thick spines which are absent only round the oral,
genital and excretory apertures.
2o8
The oral sucker, 0 025--0 034 mm. wide, lies semi-ventrally. It
is followed by the very contractile praepharynx, o*oi5--o o50 mm.
in length, which on contraction is three times shorter than when
extended. During contraction it draws the caeca upwards. The
pharynx is 0 025-0 031 mm., and the oesophagus 0 06-018 mm.
long. The caeca are short ending in front of the middle of the body
when the praepharynx is contracted, and behind it when it is
ooo
I'lo. 33. Changes in shape of Adlaia mimtissima during the movement.
extended. There is only one large oval testis 0 04-010 mm. in
length, with the long axis longitudinal. It lies just behind the middle
of the body under its dorsal surface. Behind it lies a globular seminal
receptacle 0 043-0 084 mm. in diameter. Ventrally to the testes
and seminal receptacle lies a globular ovary 0 0i8“O'035 mm. in
diameter. The latter is apparently reduced in adult specimens.
In front of the testis, behind the intestinal bifurcation and the
ventral surface of the body, lies a large globular first seminal vesicle
0 056-0 068 mm. in diameter which is connected with a second much
smaller vesicle lying ventrally or posteriorly to it. The latter is not
always present. The follicles of the vitellaria are scattered under
the dorsal surface of the posterior half of the body.
The genital aperture opens into a genital sac 0 021-0 028 mm. in
diameter. The latter is filled by a globular gonotyl which bears four
spines — two large ones 0 015-0*018 mm. in length and two half that
size. These spines project above the surface of the body.
209
The uterine coils fill the whole free space behind the genital
. aperture and often make the investigation of the internal anatomy
of the mounted preparations very difficult.
The eggs are oval, 0-024 length and 0 012-0 014 mm.
in width, and possess thick shells. They are probably seldom passed
because they were very rare in the stools of dogs even in very heavy
experimental infections.
V. REFERENCE LIST OF THE BIBLIOGRAPHY OF THE FAMILY
HETEROPHYIDAE, INCLUDING ALL SPECIFIC, GENERIC, etc.,
NAMES, ALPHABETICALLY ARRANGED
Text-books and other compilations are omitted, unless they
contain original descriptions or observations. When the original
was not available the quotations of other authors have been cited.
In preparing the following list, the Index Catalogue of Stiles and
Hassall (1908) was largely used.
ABBRliVfATlONS:
I'aust & N. = Faust and Nishigori.
IVcs. = Described in the present paper.
Stiles & 11. = Stiles and Hassall. , „
Stunkard & 11. = Stunkard and Haviland.
The figures before the colon indicate the year of the cited paper,
those after it the page ; * indicates authors who have cleared up the
synonymy ; ‘ Pres.' indicates the present paper. The hosts are
referred only to those authors who first recorded them.
Valid name
Described as
Author
Host
Adleria
Adleria
Pres.
Adlcria minutissima
j
Adleria minutissima
1
Pres.
Frlis rutus dom., Cants
familiar is ; nietaccrcariac in
Barbus canis, Varicorhinus
sp., Discognathus sp., Mugil
cephalus and M. capito.
Aduriinae
Adlerhnae
Pres.
210
\'aJicl name
Described as
Author
Host
Apophali.us
Apophallus
Liihe, 1909 ; 62
Odhner, 1914 : 224
Skrjabin, 1919 : 13
Ciurea, 1924 : 18
Ransom, 1920 : ^29,
Nicoll, 1924: 168
Stunkard & 11 ., 1924 : 6
Faust & N., 1926 : 91
Stiles & H., 1926 : 91
Pres,
/ipophallus miihlingi
Jpophallus PI uhl i ngi
Liihe, 1909 : 62, fig. 53
Odhner, 1914 : 224
Ransom, 1920 : 552, 554, fig. 20
Kotlan, 1922
Ni coll, 1923a : 168,191
Ciurea, 1924: 2, 4, 5, 10-12, 18,
figs. 2, 7, 8
Stunkard & 11 ., 1924 : 2
Szidat, 1924 : 2, 3, 4
Ruszkowski, 1925 : 175
Poche, 1926 : 148
Pres. ^
Pbahicrocorax carbo, ffiiMti-
topus himantopus, Coeblearius
cocblcarius
Larus argentatus cachiHnans^
Pelecanus otwcroialus, Canis
familiarh (c.\p.) ; nictacer-
cariac in Blicca bjorena
Fclis catus donu
Jpophallua mojor
Szidat, 1924 : 2-4, figs. la-T,
•pres.
Larus fuscus
Distoftid lingua
\
Miihling, 1898a: 21-22
Muhling, 1 898/^ ; 29, 94-96, lig- 1 6
•Jagerskjold, 1899 : 5-7
Szidat, 1924 : 2
Larus ridibundus
Distoma muhlingi
Jiigerskjdld, 1899 = 7
•Liihe, 1909 : 62 j
^ 1 c ton his oesopbagolongus
Kalsurada, 1914: 304-310, figs.
1-6, lO-Il
Ciurea, 1924: 12
Fclis catus dom. ; metacercariae
in Acerina cernua, Abramis
brama, Lcuciscus rutilus, Idas
tdus, Blicca bjorena
»
Tocotrema muhlingi
Looss, 1899 : 585
A?cotonLE
Ascucotvle (s.l.)
Looss, 1899: 584-585, 586, 611
Braun, 1902 : 30'
Looss, 1902^ : 441, 824, 832, 833
Pratt, 1902 : 888, 894
Jagcrskjold, 1903 : 14
Nicoll, 1907 ; 521
Odhner, 1914 ; 224
Skrjabin, 1919 ; 13
Ransom, 1920: 529, 561-562 •
Nicoll, 1923a : 168
Nicoll, 1923^ ; 239
Ciurea, 1924 : 17
Dollfus, 1925 : 192
Faust & N., 1926 : 91
Ascocotyle (s. str.)
•Stunkard & H., 1924 ; 2-3, 6-7
Pres.
2II
Valid name
Described as
Author
!
i Host
Ascocatyle agrense
Ascocotyle agrense
I’ravassos, 1916 ; 1-2
Ransom, 1920: 262,264
Ciurea, 1924 : 17
Viana, 1924: 97, 157
Stunkard &. H., 1924 : 3
Butoridcs striata
Ascocotyle coleostomu
Ascocotyle coleostoma
Looss, 1899 : 582, 585, 699
Ransom, 1920 : 562-563, tig, 31
Ciurea, 1924; 14,17
Stunkard & H., 1924 : 3
Poche, 1926 : 148
Pres.
i
Anoiktostoma coleostoma
Stossich, 1899/* .* 15
Distomum coleostomum
Looss, 1896^: 101-106, 154, figs.
66-68
Braun, 1901^1 : 34
Piicianus onocrotalus
Distomum colostomum
Vaullcgeard, 1901 : 143
*StiIc8 & 11 ., 1908 ; 176
Centrocestinae
Centkocestinae
Looss, 1899 : 586
Pratt, 1902 : 886, 894
Jagerskjold, 1903 : 14
Ciurea, 1924 : 17
Stunkard & 11 ., 1924 : 6
Viana, 1924: 157
Dollfus, 1925 : 192
Stiles & H., 1926 : 78, 91
Pres. ,
Phagicolinae
Faust, 1920 : 631
Poche, 1926; 153 i
*Prei.
Centkocebtus
Centrocestus
Looss, 1899 : 584, 586
Braun, 1902 : 30
Pratt, 1902 ; 888, 894
Jagerskjold, 1903 : 14
Nicoll, 1907 : 521
l.eiper, I9i3(/ 177
Odhner, 1914 : 244
Skrjabin, 1919 : 13
Ransom, 1920: 529, 559
Nicoll, I923^>: 240
C'iurea, 1924 ; 17
Stunkard & II., 1924 : 6
Faust & N., 1926 : 91
Stiles & IL, 1926 : 91
Pres.
Centrocestus cuspidatus
Centrocestus cuspida tus
Looss, 1899 : 584
Ransom, 1920': 560-561, fig. 27
Nicoll, 1923^ : 240
Ciurea, 1924: 13-17
Faust & N., 1926: 92, 121-122
Pres.
Anoiktostoma cuspidatum
Stossich, 1899^ : 15
* Looss, 1899: 582
212
V'alid name
Described as
Author
Host '
Ccntroccsius cuspidutus
Ccntroccstus cuspidatus
var. caninus
],eiper, 1 91 3<i : 176-177, i tig.
Ransom, 1920 : 561
Nicoll, 1923a : 246
Ciurea, 1924 : 17
Faust & N., 1926 : 121, 122, 124
*Pres.
Canis familiaris
Dhtumim cuspidatum
Looss, 1896: 97-101, 104, tigs.
64-65
*la)OS8, 1899 : 576, 581, 584
Braun, 1901a : 34
Mil'i'us piirusiticus
CtllCAKlOlDt.S
C’ERCAKIOlDtS
Pres.
(U:rcii r ioi d cs aba run i i
L'vrairioidi's aharoni i
Pres.
Pu§inm kuhli
Cekcakiuiuinal
Cekcauioidinae
Pres.
CBVrTOCOTVLE
Cryi'Tocoi LE (partim)
Lulie, 1899 =
l.ooss, 1900 : 607
Luhe, i90o/>; 557
Braun, 1900 : 6
Braun, 1901a : 56
Jagcrskjold, 1901 : 981
Pratt, 1902 : 888
Luhe, 1909 T 87
Ransom, 1920 : 527, 529
Maplestonc, 1922 : 155 ,
Issaitschikoff, 1923 : 1, 3, 4.
Nicoll, 1923a : 168
Ciurea, 1924 : 1,18
Stunkard & H., 1924 : 6
Faust & N., 1926 : 91
Stiles Sc 11 ., 1926 : 90
Poche, 1926 : 147
Ckvi*t(>c«t\le (s. vStr.)
Nicoll, 1907 -
Nicoll, 1909 : 483
*Prc8.
CujREANA
Skrjabin, 1923 : 6
Issaitschikoff, 1923 ; 1, 3, 4
*Prc8.
'I'ocoTKEMA (partim)
see 'Focotrema (partim)
l^ryptucotyh’ cuncuvum
Cry p tocolyl c conawim
Luhe, 1899 : 539
Fischoeder, 1903 : 548
Nicoll, 1907
Nicoll, 1909 ; 483, 484, tigs. 22, 23
Liihe, 1909 : 87-88, fig. 71
Ciurea, 1915a : 446
Nicoll, 1915 ; 360
Ransom, 1920: 544, fig. 11
Nicoll, 1923a: 168, 179, 182, 184,
191, 192, 193
IssaitschikoflF, 1923 : 3-4, fig. 2
Ciruea, 1924: 13, 18
Issaitschikoff & Weinberg, 1926 ;
305-308
Pres.
.
Lams hypirburcus, Colymbus
nigrkollis
Mctacercariae in Plcuronectcs
platcssa
Nyroca fuligulu, Oidemia nigra
Felis cam dom.^ Cams
familiaris, Rattus mrvegicus ;
metacercariae in Traeburus
trachurus
Valid name
Described as
Author
Host
Cryptocotylc concavum
Distoma cuncavum
Crcplin, 1825 : 45-47, 83 ; figs. 7, 8
Crcpliii, 1837; 310,314,318
Dujardin, 1845 • 44 ^
Creplin, 1846: 138, 141, 145, 14O
Diesing, 1850: 340-341
Cobbold, i860 : 11
Stossich, 1892^ : 158
K-Owalcwski, 1895 : 2 (350)
Itraun, 1893U : 874-879
Slossich, i898<i ; lo
Stossich, 1898^ : 42
Miihling, 1898/*: 4, 19-24, 27,
80-83, fig'** fi) -fi
*Luhc, 1899 : 539
Jagerskjold, 1899 : 9, 10, 12, 14, 16
Jacoby, 1899 : 22-23
Looss, 1899 : 586
Looss, 1900 : 607
Braun, 1900 : 6
Braun, 19014- : 564
Cavia stcllata
(.’olymbus c/istalus, Aha torda,
Anus hurnschuchi, (Haiuion
iiangiila, Claiigiilu hvcmalis^
Fuligula marilu, Mdanitta
fiisca^ Mcrgus scrralor^
3 1 crganscr merganser
(.'olymbus nigricollis
Toiutu ma lOiiLavuin
(.0088, 1899 : 586
Kowalewski, 1902 : 26
jagerskjold, 1903 : 3, 4, 5, 11, 13
l*huluet oeurax aristotcUt
Ctyptocofylc cryptutuly-
luidcs
Cryptoiulylc cryplotuty-
loidcs
Pres.
•
Cittnanu cryptofoiyloida
Issaitschikoll, 1923: 1-4, ligs. 1-3
•Pres.
Colymbus anlicut
Cryplatuiyle
(juinqueuti^ulure
Cryptocotylc
ijtiiiiqucangularc
Pres.
Ciurt'una quinqucangularc
Skrjabin, 1923 : 4-6, lig. i
Issaitschikoff, 1923 : 3, 4, lig. 4
•Pres.
lulls CdlUS dom.
CRVPlOCOlYLiA
Ckyptocotylea
Pres.
Apophallinac
Ciurca, 1924 ; 17
Stunkard & 11 ., 1924: (»
Stiles & 11 ., 1926 : 91
•Pres.
CKYriOCOlYLlNAi:
Liihc, 1909 : 86
Ciurca, 1924 : 18
Stunkard & 11 ., 1924 : 18
Stiles & H., 1926 : 81,91
•Pres.
JI’ocorKiiMiWAi!;
Jiigcrskjdld, 1903 : 14
Nicoll, 1907 : 483, 484
Poche, 1926 : 147
•Pres.
I^EXIOGONIMUS
Dexiogonimus
Pres.
1
214
\’alid name
Described as
i Author
Host
Dexiogonimus ciun anus
Di'xio}>animus ciurcanm
1
j Pra.
1
1
i
i
Felts catus dom., Cams
familiaris, Larus sp. ; meta-
ccrcariae in Tilapia simonhy
T. galilca, Discognathus sp.,
Barbus cants, Mugil cephalus,
M. capita and Lichia glauca.
DlOKCHlTRKMA
! DlOKCHlTRKMA
1 Pres.
Diorchitrma
pseudocirralu
; Dionbitrcma
pseudocirrata
1
: Pres.
Fdis catus dom., Cants
familiaris ; nictacercariac in
Mugil cephalus, M. capita.
Galactosomlm
Galactosomuai
!
1
i
: l.uuss, : 671
! Looss, 1 902 : 5 1 2
Pratt, 1902 : 890, 91c
J iigcrslcjold, 1 908 : 3 1 b, 3 1 7
Odhncr, 1910: 354, 356
Pratt, 191 1: 143-148
Nicoll, 1923^ : 168
Poche, 1926 : 152
Pres.
Oalactosomum erinaccum
j Gulactoiomutn t rinauum
Jagerskjdld* 1908 : 317
Nicoll, 192341 : 240, 244
Pres. 1
1 Dutomum ennuccum
\
\
Poirier, 1886 : 37, 38, fig. (>
Braun, 1893 : 643-870
Monticclli, 1893 : 83, 86, 103, 106,
I 107
1 Looss, 1899 • 590
hjagcrskjold, 1908: 317
Iklpbimis ddphis
•
Cdlactosomum luett um
Galactomnum lach um
:
j Looss, 1899 : 671
1 Looss, 1902&; 512
J iigerskjold, 1908: 31 6-3 1 7
Odhncr, 1910: 334-356
Odhncr, 1911: 181 j
Nicoll, 1915: 349, 354, 364 1
Nicoll, 1923(1 : 168,179 1
Pres.
Fhalacrocurax carbo
Metacercariae in Cottus bubalis
Distomum hemicidum (?)
I
Moliii, 1859: 829,830
Carus, 1885: 127 ;
Stossich, 1886: 43
•Odhncr, 1911 : 186
Poche, 1926; 152
Pres,
Bdone ucus.
Moiiostomum lacteum
Jagerskjuld, 1896: 165, 167-177,
figs. 1-8, text-fig. 1
Jagerskjuld, 1899 ; 15
•Looss, 1899 ; 671
Braun, 1899(1 : 724
. Jagerskjuld, 1900: 736
•Braun, 1901(1 : 47
Ward, 1901 : 180
McLaren^ 1904 *583
Jagerskjuld, 1908: 316" |
Metacercariae in Cottus scorpius
Valid name
f
Described as
i
Author
Host
Haplorchinae
IIaplorciiinae
Pocho, 19^6 : 152
Pres.
Haplorciitinaf,
Looss, 1899 : 671
*Pocho, 19’h:
1
1 IfAPrORCHH)INAE
1
Pratt, 1902 : Hip
*Pochc, 1926; [52
j Monorchitreminaf.
Nishigori, 1924
Faust & N., 1926 : 124
*Pres.
IIapiorctiis
Hapiorchi?
Looss, 1899 : 670, 671
Looss, 1902/^ : 442. 512
Pratt, 1902 : 890, 910
McCalluni, 1902 : tilT)
Pochc, 1926 : 152
Pros.
i
I
1
1
Haplorchin enhirinus
j flaplorrhis cdhirinua
Looss, 1899 t 671, 7:12-7 41, fig. 89
Odhncr, 1910 : 31^5
Pres.
llaprus (iocmac
Disimum cahirinim
Looss, : 1 19-1 12, figs. 8.|
*Loos8, 1899 : 752
Biipru^ hayad
Haplorchis pumilio
Ilaplorrhis pumilio
Looss, 1899 : fi7i, 753
Pres.
•
Monostomum pumilio
T.ooss, 1896/): i;;4-iq8, figs. loi-
106
•Looss, 1899 : 670, 741
Ciurea, 1924 : 3
Poche, 1926 ; 152
Prlcronun onocrotalus^ Mihus
(ii’yyptiH^
Heterophyea
Heteropiivea
Pres.
Heterophves
ITeterophyes
Cobbold, 1866 : fi
Stiles & 11., 1900 : 563
Looss, 1902^ : 886
Looss, i902/» : 786, 804 808, 824
Odhncr, 1914 : 244
Skrjabin, 1919 : 13
Ransom, 1920 : 327, 329, 43c'
Nlcoll, i923/> : 239
Ciurea, 1924 : 17
Stunkard & IL, 1924 : 6
Faust & N., 1926 : 91
Pres.
COENOOONIMUS
Looss, 1899 : 585, 386, 619
Looss, 19CK) : 608
Ofenheim, 1900 : 183
Jiigerskjold, 1900 : 736
Odhner, 1900 : 21, 21
Liihe, i90oi»: 557
•Stiles & IL, 1900 : 563
2i6
Valid name
Described as
Author
Host
ITkteroi'hyf.s
COENOOONIMITS
CotYI OGONIMUR
Braun, 19014 : 56
Braun, 1901^ : 334
Braun, 1901^ :
Loobs, 19024 : 886
Loofls, 1902/^ : 832, 835
JagcrBkjold, 1903 : 10, it, 13, 15
Liihe, 1899 : 538, 539
Lube, 1900A : 555, 557
Loosb, 1900 : 607
Braun, 1900 : 6
Braun, 1900^ : 56
'•StileB & H., 1900 : 563
Braun, 1901^ : 334, 338
Loobb, 1902^; 813, 833
Pratt, 1902 : 888
Stunkard & H., 1924 : 6
IJetrrnphyrs nrqunlis
Ilcicrophyrs aequnlh
Loobs, 19024 : 888
Hall & Wigdor, 1918 : 237
Ransom, 1920 : 531, 535, 536
Skrjabin, 1923 : 4
Nicoll, 1923/; : 239, 245, 246
Ciurea, 1924 : 13, 17
Pres.
*
i
Frlis catus dam., Canis
familiaris,
Persian wolf ; mctacercariac in
Mugil eephalus, M. capita^
M. auratus^ Kpinephelus
enaeus^ Tilapia stmonis, JAchin
nmia^ L. glauca .and Barbus
cams
Distomiim frntcruum,
parlim
1
1.0088,18944: 42-48, figs. 13-15
Looss, 1 896/1 : 60-63, loi, J54,
1 56, figs. 36-37
Sonsino, i^i)(d): 314
Miihling, 1898/1: 81-82
Stossich, i898/>: 42
I.00S8, 1899 ; ' 535 , 550, 556
Jagerskjbld, 1899: 9, 12
Liihe, 1899: 539
Jacoby, 1899 : 23
Braun, i90i/> : 334, 336, 338
1.0088,19024: 886-887
*Prcs.
•
JictFrophycs imps
Loobs, 19024 : 887-888
Ransom, 1920: 535
Ciurea, 1924 : 13, 17
•Pros.
Prlccamis onocroialus, Mihus
aegyptius.
If etnnphyes dispnr ■
[ Ihlnophyrs dispar
\
Looss, 19024 : 888, 890, 891
Hal! & Wigdor, 1918 : 237
Ransom, 1920 : 536-537
Skrjabin, 1923 : 4
Nicoll, 1923A : 239, 245, 246
; Ciurea, 1924 : 13, 17
i Pres.
Felis catus dm., Canis
familiaris
Persian wolf ; metacercariae in
Mugil cephalus, M. capita^
M. auratus, Epinephelns
enaeus^ Tilapia simtiist
Licbia amia^ L. glauca and
Barbus cattis
Valid name
Uetcraphyn d I spar
lirtcrophyes hrterophyes
2i:
Described as
j
Author
Host
IJcterophyes dispar
Looss, I902tf : 890, 891
limatus
Ransom, 1920 : i;;^7
*Pre8.
Distommn fratrrnum,
Looss, 1894^: 42-48, fij2S, i vit;
prirtiin
Looss, 1 896/j : ^0-6'?, lor, 1-4,
156, figs. 36, 37
Sonsino, 1896 : 314
Miihllng, 1898^ : 81, 82
Stossich, 1898/* ; 42
1.0088,1899: 5355550,
Jiigerskjold, 1899 : 9, 12
Luhe, 1899 : 539
Jacoby, 1899 : 23
Rraun, I90ii^ : 334, 336, 338
Looss, 190247 : 886, 888
*Prcs.
j llrtf'rophvi's hrirrophves
Stiles & H., 1900 : 563
i
!
T.ooss, 190247 : 889, 8go
Man, FrJis rntus dom.^ Canh
JamHiai is
1
1.0098, 1902/7: 782, 785, 786, SnS,
809, 838, 854
Ciurea, 191541 : 453
Hall & Wigdor, 1918 : 237
Ransom, 1920: 531-533, figs, i, 2
Cort &. Vokogawa, 1921 : 68, 69
Skrjabin, 1923 : 3
Nlcoll, i923/>: 239, 245, 246
Kobayashi, 1923 : 97-98, fig i
Metacerenriae in Mugii 8]’>.
Khalil, 1923 : 141-142, fig, 13
Ciurea, 1924 : 13, 17
I'aust & N., 1926 ; 91, 92, 122, 123
Stiles & IL, 1926 : 92
Poche, 1926 : 148
Cram, 1926 : 43
Chapin, 1926 : 37
NicoIJ, 1928 : 339, 344,, 343, 3 |6
Metaeerenriae in M iigil rrp/vilus
Pres.
Kvperim. rabbit, (Jirrnrtiis
gallirus ; inolacercariae in
Mugii capita^ M. nuratus,
Kpinephidus eiiaeus^ Tl/apia
siffionis, TAchia a win, 7 ,. gin urn
and Unrhus rnuis.
C } i ms iomum heterophyes
Raillet, 1898 : 173
Comogonimus fraternus^
Looss, 1899 ; 585, 700, 701
parfim
Looss, 1901 : 205
Jagcrskjold, 1903 ; 3
•Pres.
Coenogonimus heterophyes
1.0088,1899: 578, 585, 586, 699,
700, 701
•Stiles & IL, 1900 : 563
Jiigerskjold, 1903 : 3
Pres.
- - . --
. . - ^
_ _
2I8
V^'jlid name
Described as j
Author
Host
j
Hf'tt'rophvc^ hftnopbvi'Si j
(^otvlogonimus framnus^
par rim
Liihe, 1899: 539
Braun^ 19013 : 337
Fischoeder, 1903 : 548
Ransom, 1920 : 534
•Pres.
Cotyhgonimm hrinophyes
Liihe, 1899 : 539
Braun, 19013 ; 331;, 337, 338
Fischocder, 1903 : 1548
* 1 . 0068 , i902<i ; 886
Cotyla^onimus persicus
Braun, 19013 : 334-338, fi/?. 13
Braun in Looss, I902 <j : 891
Ransom, 1920 : 537
•Pres.
‘ Persian wolf.’
Dicrocoelium hftfrophyes
Weinland, 1858 : 86
Cobbold, 1856 : 6
•Stiles & H., 1908 : 151
Dhtomum fratcrmtm,
pnrrim
Looss, 1894/1: 42-48, 6^6. 13-15
Muhling, 18983 : 81, 82
1.0088,18963: 60-63, 10 1, 134,
*56, figs- 36-37
1.0088,1899: 535) 550,35^’
Jacoby, 1899 : 23
Jagcttkjold, 1899 : 9, 12
I.iihe, 1899 : 539
Braun, 19013 : 334, 336, 338
Looss, 1902/7 : 886, 887
•Pres.
Pekeanus onocroialus
Distomn hetcrophyea and
Distoma hcft'ropbyrs
homittis
For the exhaustive references, see :
Stiles & IL, 1908 : 199; note
•Stiles & IL, 1900 : 563
Fasciola hetrropbyrs
Moquln-Tandon, i860 : 343
•Ransom, 1920: 531
fhtnophycs aci^yptiaca
Cobbold, 1866 ; 6 ^
Stiles & H., 1900 : 563
H r trropbyrs f ra fcrnus,
partim
Looss, 1902/7 : 887, 888
Looss, 19023: 783, 808, 809, 838,
854
Looss, 1907 : 488
Ransom, 1920 : 534, 535, 536, fig. 3
Nicoll, 19233 : 239, 245, 246
Ciurea, 1924: 13,17
•Pres.
11 Pterophycs helcrophyrs
scntus
Looss, 1902/1 ; 890, 891
Ransom, 1920 ; 533
•Pres.
Hetcrophyes pallidus
Looss, 1902/1 : 889, 890
Ransom, 1920 ; 533, 534
Ciurea, 1924-^-27 !
•Prcfl.
Milviis aegyptius
219
Valid name
Described as
Author
Host
Hetcrophyes hetPtophyrs
Ihteropbyrs prrsirus
Bmun in LooiJs, igoztf : 8t)i
Looss, 1902^ : 782, 785
Ransom, 1920 : 5;^7, lig. 4
Poche, 1926 : 147
Cram, 1926 : 43
*Prc9.
Mesorinnimus hpfrrnphyn
Raillet, 1890: 143
Stossich, i892/> ; 31, 32
Monticclli, 1893: 89, I5fi
Ward, 1895 ; 328
Blanchard, 1900 : 488
lieterophyex mcens
.
\\
Uetnophyps mrcm
Onji, 1915 ; 875-883
Onji & Noshio, 1915 :
Cort, 1921 : 187
Cort & Yokogawa, 1921 : 66-69,
figs. 1-5
Lane, 1922 : 505
Ciure.a, 1924 : 13, 17
Stunkard & II., 1924 : 2
Kalsiirada, 1925 : 2
Faust & N., 1926 : 92, 122
Nicoll, 1928 : 345
Pres.
Man ; metacercariae in Mu^il
ct'phajiis, M. j(ipoiucu<!
Jlcterophyra hrtrrophycs^
part.
Janson & Tokishigc, 1892 : 3 50
Janson, 1893 : 265
Leiper, 19I3<3 : 176
Nicoll, 1928 :
Ileterophyn kaisuTodai
Ozaki & Azada, 1926: 216-218,
fig. I
Azada, 1926 : 360-365, figs. 1-4
Nicoll, 1928 : 345, 376
•Pres.
Cams familiaris
Mfsnponiniin hrtrrophyes
Raillet, 1890 : 143
Stossich, 1892A : 31-32
Ransom, 1920 : 531
•Ciurea, 1924 : 13
Faust & N., 1926 : 122
Heterophyipae
Ilr.TEROPHYIDAF,
Odhner, 1914 : 224
Skrjabin, 1919 : 13
Ransom, 1920 : 528-52()
1'ravassos, 1921 : 85
Nicoll, I923<J : 168
Nicoll, 1923A ; 238
Ciurea, 1924 : 16, 18
Stunkard & H., 1924 : 6
Dollfus, 1925 : 192
Faust 1926; 91,92, 121
Poche, 1926: 147, 163
Stiles & IL, 1926 : 90, 91
Chapin, 1926 : 37
Pres.
Aplorchipae
Viana, 1924 : 107, 149
•Poche, 1926 ; 147
220
Valid name
Described as
Author
llrrfKOPlTVIPAF
CoKMOr.ONIMIDAF-
Nicoll, 1907 : 261
•Pocho, 1926 : 147
CnTvr onoNiMiDAF.
Nicoll, 1907 : 26r
*Poche, 1926 ; 147
IlArrORCIIIDAE
Travassos in Vinna, 1924 : i ijc)
*Pnche, 192b : 147
Stictodohidaf.
Poche, T926 :
•Pres.
IlKTF.KOPHVmAE
Hetf-rophyinaf
Ci urea, 1924 : 17
Stunkard, 1924: b
Dollfus, 1925 ; 195
Pres.
CpENOnONIMINAF
Looss, 1899 : 586, 610
Odhner, 1900 : 21, 23
Odhner, 1905 : 3^4
Nicoll, 1909 : 484
Stunkard & H., 1924 : 6
COTYLOnONIMINAE
Pratt, 1902 : i88
•Stunkard & H., 1924 : 6
Mftaconimtnae
Ciurea, 1924 : 17
Stunkard & 11 ., 1926 : 6
Stiles & IT., 1926 : qi
MtTAGONlMtJS
j
MeTACONIMI'S
i
1
Katsurada, I9i2r
Vokogawa, I9I2<J
Yokogawa, i9i2/>
Yokogawa, 1913^
Ciurea, 19 iijZ* : 112
Skrjabin, 1919; 13
Ransom, 1920: 527, 529, 538, 339
T.eiper, 1922 ; 364-365
Ciurea, 1924 : 3, 4, 17
Stunkard & II., 1924 : 6
Nicoll, 1924 : 131
Dollfus, 1925 : 195
Poche, 1926 : 147
Stiles & IL, 1926 : 90, 91, 92
Nicoll, 1928 : 345
Pres.
Loossia
Ciurea, I9i5fl: 454-455
Ciurea, 1915A : 112
•Ransom, 1920 ; 527, 340
Ciurea, 1924 : 4
Loxotrema
Kobayashi, 19120 : 785
Kobayashi, 1912^’: 607
Leiper, 1922 ; 364, 365
Nicoll, 1923^ : 239 j
•Dollfus, 1925 : 195, 196 [
Faust & N!, 1926 : 92, 123 |
Stiles & H., 1924: 92
Poche, 1926 ; 147 1
221
Valid name
1 Described as
Author
Host
Metagonimus
! Yokogawa
!
Leiper, 1913 : 282
•Ransom, 1920 : 527, 539
Faust & N., 1926 ; 123
Stiles & H., 1926 : 90, 92
Metagonimus romanicm
I Mctngnmmm romnnirus
Ciurea, 1924: 4, 5-10, 17
Stunkard & 11 ., 1924 t 2
Pres.
Lnosun dohrogirnsis
Ciurea, I9i5<i ; 454
Ciurea, 1915/; : 108-112
•Ransom, 1920 : 38, 42-43
Ciurea, 1924 : 3-4
Pejeennus nnnrrnfajus
Imma parvn
Ciurea, I9i5<2 : 4<?3-434, fig. 6
Ransom, 1920: 538, 541-542,
fig. 10
•Ciurea, 1924 : 4
Felis cams dom. ; metacer-
cariae in Esox hirii/s
Lonssid rnmanira
Ciurea, 1915/7: 446-453, figs. 1-3,
text-figs. 1-3
Ciurea, 1 91 5/^ : 109- 1 1 2
•Ransom, 1920 : 538, 541, figs. H, (f
Hall & Wigdor, 1918 : 237
Ciurea, 1924 : 4
Stiles & 11 ., 1926 : 90, 92
Felis cams dom.^ Canis
f ami liar is^ Sus scrofa dom.,
Peleratiiis ouorrntaltis ; meta-
cercariae in Esox Indus,
Scardi ui us erythrophthal mus,
dhramis hr am a, (hirassim
carassiiis, /hpius aspius
Metagonimim dohrogirnsis
Ciurea, 1924 ; 3-4, 13. 17
•Pres.
i MHagonimua parvm
Skrjabin, 1923 : 4
•Ciurea, r924 : 4
Metagonimus yohogatvai
(partim)
Nicoll, 1924: 129, 135, 136, 137,
‘38 .
Faust & N., 1926 : 123
Mftngommua yokogarvai
: Metagonimus ynkogawai
\
Katsurada, I9i2r
' Vokogawa, 1912/7
Yokogawa, igtz/f
Katsurada, 1913 ; 49-77, figs, i-r q
Yokogawa, 1913/^
Yokogawa, I9i3<y: 158-179, figs.
T-17
Ciurea, i9i5/> ; 108-112
Muto, 1917/1: 115
Muto, igjyd : 79
Ransom, 1920; 538-543, figs. 5-9
Cort, 1921 : 187
•T.eiper, 1922 : 364-365
Ando, 1922 : 1,2,4-9,21,22
Ciurea, 1924 ; 4, 7, 8-10, 17
Nicoll, 1924: 151, 13s, 136, 137,
138
Stunkard & H., 1924 : 2
Dollfus, 1925 : 195-196
Faust &N., 1926 : 92, 115-116, 120
[Stiles & II., 1926 : 92-93
Nicoll, 1928 : 339, 343, 344, 345,
34 ^’
Pres.
Metacercarine In Carassius
aureus, Leudseus halueusis
Cercarlae in Melania libertinn
Chimarregale platycephala, Mus
molossinus, Raitus ratms,
Rattus norvegicus
1
! i'
j 1
i
!
Record following molluscan
hosts : Katayama nosophora,
Melania ebenina, M, extensa,
M. gottschei, M. nodiperda-
quinaria, M. obliquegranosa,
Pyradus cingula tus
222
V^alid name
j Described as
1
Author
1
Host
MrtO'^on imus vokfipatoai
Mctagomnmyokn^awai
j (partim)
Nicoll, 1924: 129
Fansr & N., 192b : 123
i
Hcferophycs rlJipfica
Yokngawa, T9I3<7
II cfrrnphvcs yoh»a 7 rai
Katsurada, r9r2^7
Katsurada, 1912/)
*f)ollfus, 1925 : 195-196
Man, Felix catus dortt., Cams
! familiarix ,* metacercariae in
! Plecof^lossus aliivelis
Loxoircma ovaltm
•
Kobayashi, T9T2<7 j 785
Kobayashi, 1912A : 607
helper, 1922 : 364-365
Nicoll, 1923^ ; 239, 246
•Dollfus, 1925 : 196
picia^nnimm ovatus
Yokogawa, 1913^: 45-49, figs. 1,2
•Ransom, 1920 : 53K, 540, fig. 7
Poche, T926 : 148
7 ncritrrmn yokofiaiva
Leiper, I9I3A: 282
Tokna^arca vokogamj
helper, 1913^ : 176
helper, 1913^^ 282
•Ransom, 1920 : 538
Stiles & Ih, 1926 : 90, 92
MfCROMSTHUM
Mtcroi istkum
Braun, I90if : 563, 895
Braun, 1902 : 55
Pratt, 1902 : 889
Odhner, 1910 : 354, 356
Pratt, 1911 : 143
Nicoll, I923<i : 168
Pochc, 1926 : 1 52
Pres.
■
Galactosomum
Pratt, 1911 : 143-148
Poche, 1926 ; 152
•Pres.
Microlhtrum cochlear
MicroHatrum cochlear
1 Braun, 1901c; 563
Braun, 1902 : 56-58, fig. 36
Odhner, 1910 : 353-356, fig. \
Nicoll, 19230 ; 168,192
Pres.
Distomum cochlear
Dicsing, 1850 ; 357, 358
Creplln, 1851 : 288
Cobbold, i860: 14
Stossich, 18920; 179
•Braun, 1901c: 561, 563, 895
Braun, 1902 : 56, 58
Sierva sandwichensts, S. minuta
\ Dhlomnm cochleari forme
(partim)
Rudolphi, 1819 : 681
Dujardin, 1845 : 449
•Braun, 1901 : 893, 895
Braun, 1902 : 55, 56, 58
Distomum coeblearijorme
sternae (partim)
Diesing, 1850 ;J57
Cobbold, i860 ; 14
223
Valid name
Described as
Author
M i aol is trum cochlear
Distoma dicsin^i
Cubbold, )S6o : 14
•Stossich, iSyi : 179
Braun, 1901c : 561, 564
Braun, 1902 : 56, 58
(Jalactosomum cochlear
Pratt, 1911 : 143, 148
Viana, 1924: 106, 107, 159
Sleruii iiutillarum
M icol i strum cochlear i-
Jormc
M icrolistrum cochlcari-
forme
Braun, i90it : 563
Braun, 1902 : 56, 58, fig. 35
Odhncr, 1910: 353-35O
Nicoll, 1923 : 168, 192
Pres.
[
Distomum cochlcari forme
(parliiTi)
Rudolphi, 1819: 681-082,6871 h'rcpala (uptila
Dujardin, 1845 : 449
Dicsing, 1850 : 357
Stossich, 1892^ : 179
•Braun, 1901c ; 561, 563, 895 ;
Braun, 1902 : 55, 56
Distomum cothlearijorme
slcrnuc (partiin)
Diesing, 1850 : 357
Cobbold, i860 : 14
Cialaciosomitm cochlear i-
forme
Pratt, 1911 ; 143, 148
Viaiia, 1924 : 107, 159
•Pres.
M icf olistrum s cm if uscum
M icrolistrum scmijuscum
Pres.
Calactosomum semif uscum
Jagcrskjold, 1906 ; 316, 317
Nicoll, 1923^ : 168
•Pres.
Monuslomum semijust um
Olsson, 1876 : 28, ligs. (>5, 00
Braudes, 1892 : 505, 509
Monticelli, 1892 ; 706, 710
Braun, 1893 : 916
•Jagcrskjold, 1908 ; 317
Odhiier, 1910 : 35O
t^ula hdsana
M icrolistrum sp i n c i u m
MicroHstrum spiuctum
Braun, 1901c : 563, 895
Braun, 1002 ; ‘59-62, figs. 37- 59
Odhner, 1910: 353, 355, 356
Rhyiuhvps nigra
Calat losomum cochlcari-
forme
Linton, 1928 : 23, fig. 52
*Pres.
fregata magiijuc
Calactosomum spiuctum
Viana, 1924: 149, 159
•Pres.
Monorchitkema
Munokcuitkema
Nishigori, 1924 '.569
Faust & N., 1925
Faust & N., 1926 : 93
Pres.
224
V^jilid naiiu:
Monorchitrma taihokui
Mumrdntrmu tuthui
I'akascocotvu
Described as ! Author
Host
Momrehitrema taihokui
Nishigori, 1924 ; 569
Faust & N., 1925
Faust & N., 1926 ; 93-125, figs. 1-5,
12-19, 25, 27, text-fig. I
Nicoll, 1928 : 340, 345, 346
j Molluscan hosts : Melania
reiniana var. hidachiens ;
I secondary hosts : Carassius
i auratus, Clarias fuscus^
Cbanna f&rmosana^ Pseudas-
bora parva^ Phoedeus ocellatus,
Gatnbusia affinis^ Polycantbus
operculatus, Ctenopbalus tadi-
anui, Misgurnus anguilli-
I caudatus, Parasilurus asotus^
j Zacco platypus^ Cyprinm
i carpio ,• definite hosts :
Nyciicorax nycticorax^ Felis
catus dom.^ Canis familiarise
rabbit, mouse, guinea-pig. .
Mononhtlrcma iaihui
Parascocoiylf,
I Pres.
Nishigori, 192^ : 569
Faust & N., 1925
Faust &; N., 1926 : 93-125, figs. 2,
6-11, 2Q-22, 26, 28
j Nicoll, 1928
I Pres.
I Stunkard & H., 1924 : 3, 4
j Dollfus, 1925 : 192
j Pres.
Metaccrcariae in Tilapia nilo-
ticue T. galilea, T. simonis,
Barbus longicepSy Mugil
, capita, M. cephalus, Barbus
canus ; adults in Larus sp.
Ccrcarlae in Melania oblique-
granosa ; metaccrcariae in
Cyprinus carpio, Carassius
auratus, Zacco platypus,
Pseudasbora parva, Phoedeus
occllatus, Gambusia ajinis,
Cienopharyngodon idellus ;
adults in ‘birds, mammals,
including man.’
I Felis catus dom., Canis
I familiaris, Larus sp. ; meta-
j cercariae in Varicorhinus sp.,
j Barbus canus, T ilapia simonis.
Ascocotyle (partini)
1 1.0088, 1899 : 584, 585, 586, 611
Braun, 1902 : 30
Looss, 1902^ : 441, 824, 832, 833
Pratt, 1902 : 888, 894
Jagerskjfild, 1903 ; 14
Nicoll, 1907 : 521
Odhner, 1914 ; 224
I Skrjabin, 1919 : 13
' Ransom, 1920: 529, 561, 562
! Nicoll, 1923d ; 168
! Nicoll, 1923^: 239
Ciurea, 1924 : 17
l*Stunkard & H., 1924 : 2, 3, 6, 7
I Pres.
PHAGICOLA I Faust, I920 ;
|*Faust & N., ^4 1) 93 -
' Poche, 1926 : 15!, .53
225
Valid name
Described as
Author
Host
Paruscocotyle ascolonga
PurascocotyU italica
Parascocoiylc ascolonga
Purascocutylc italica
Pres.
Stunkard & 11., 1924 : 3
Pres.
P'clis cat as dow., Canis
familiaris ; melacercariae in
T ilapia simonis.
Ascocolyie italica
Alessandrini, 1906 : 221-224
Hall & Wigdur, 1918 : 237
Ransom, 1920 : 262, 263, 264, 2O8
Nicoll, 1923^ : 239, 246
Skrjabin, 1923 : 4
Ciurea, 1924 ; 14, 17
•Stunkard & H., 1924 ; 3
Eanis jamiliarls
Eebinostomum pyriformc
Nicoll, 1923Z» : 239
Plane & lledin, 1913
•Skrjabin &. Lindlrop, 1919: 6
Puruscocolyle langa
Paruscototyic lottga
Stunkard & 11., 1924 : 3
Pres.
Ellis catus ilotn., Canis
familiaris^ Persian vvoH ;
metacercariae in Mugil
ccphalns, M. capilo, Licbia
amia, Barbus canis.
Ascototylc longu
Ransom, 1920 : 5()4-5()(), lig. 29
Ciurea, 1924: 14,17
•Stunkard & 11., 1924 : 3
Cram, 1926 : 43
I 'ulpcs lagopus
Purascuiulylc minutu
Purascocutylc: minula
I Stunkard &. 11., 1924 : 3
Dollfus, 1925 : 192
Pres.
\
Ascocotylc minuta
1
i
i
1
Looss, 1899 ■: 585, 698-699, 7U0,
701, lig. 23
Looss, I90ifl : 205
Faria, 1910: 287
Railliet & Henry, 1913 : 930
'I'ravassos, 1916 : i
Hall & Wigdor, 1918: 237
Ransom, 1920 : 532, <^38, fig. 28
Nicoll, I923<2 : 168, 185
Nicoll, 1923^ : 239, 246
Skrjabin, 1923 : 4
Joyeux, 1924 : 3
Viana, 1924: 134,15?
Ciurea, 1924 : 14, 17
•Stunkard & H., 1924 : 3
Dollfus, 1925 : 192
Eiiis latus dom., Canis
Jamil iatis^ Anica Lincrca
Parascocoiylc diminuta
Stunkard & 11., 1924 : 4-^, lig. 1
Dollfus, 1925 : 192-194, fig. 1
•Pres.
liattus norreguus
Parascocotyie nanu
Parascocoiylc nana
Stuncard & H., 1924 : 3
Pres.
Ascocotyle nana
Ransom, 1920: 562, 566-568, fig. 30
Ciurea, 1924: 14,17
•Stunkard & H., 1924 : 3
Cram, 1924 : 3
Eulpcs lagopus
Valid name
Described as
Author
_j
Host
Parascocutylf pithcco-
phagicola
Parascocotyle pitheco-
pbagicola
Pres.
Aicocolylc pitbecophagicola
Faust & N., 1926 ; 83, 123
•Pres.
Phugicola pitbecophagkola
I'aust, 1920 : 630-631, tigs. 4-6
•Faust & N., 1926 ; 92, 93
Poche, 1926: 153
Pitbecopbaga jeffreyi
PyoiDiopsis
PYGimopsiti
Looss, 1907 ; 488-490
Odhncr, 1914 ; 244
Skrjabin, 1919 ; 13
Ransom, 1920 : 529, 568
Stunkard & H., 1924 : 6
Ciurca, 1924 ; 17
Faust & N., 1926 : 91
Py^idiopiis genuta
Pygidiopih genata
Looss, 1907 ; 488-490, tig. 7 '
Ransom, 1920
Ciurea, 19^4: 2, 3, 13, 17
Faust & N., 1926 : 93, 122, P24
Pres.
PeUcanus unucroialus
Cants fumtiiuris, lulls catus
dom,, Persian wolf j nieta-
cercariae in Tilapia simonis,
T, galilea and Barbus canus.
j Aicocotyle plana 1
Linton, 1928 : 20, 21, tig. 50
•Pres.
Butoridcs virescens
RoWICOTKtMA
* RoSSICOTKtMA
Skrjabin, 1919 : 13, 14, 17
Ciurea, 1924 : 14
1 SdJes & JI.,' 1926 ; 91
’ Faust & N., 1926 : 92
Pres.
: CoTYLOPHALLUS
Ransom, 1920: 529, 554, 555
IMicoll, 19236 : 240
Szidat, 1924 : 3, 4
rCiurea, 1924 : 3, 4
Stunkard & H., 1924 : 6
Faust & N., 1926 : 92 '
Stiles & H., 1926 : 91
Pres.
Rossicotrma donicum
Kossicotrmth donicum
Skrjabin, 1919; 14-16, tig. i
Skrjabin, 1923 : 4
Ciurca, 1924 ; 4, 17, hgs. 3, 4
Pres.
Fiiis catus dom., Cants
familiaris
Metaccrcariae in bcardinius
erytbrophtbalmus, Abramis
brama^ Blicca bjbrcnu.
Apopbdlus brevis
Rpsom, 1920 : 553, 554, tig, 21
Ciurea, 1924 ; 14, 18
Szidat, 1924 : 2, ^ 4
Poche, 1926 : 148
•Pres.
tarus delavarensis
227
Valid name
Described as
Author
Host
Hossicotrmu donkum
Cotylopballus similis
, Ransom, 1920: 555, 558, 559,
fig. 26
; Nicoll, 1923/* : 240, 243
; Ciurea, 1924 : 14
|*Pre8.
Pboca vilulina
Colylopballus venustus
Ransom, 1920: 555, 558, 559,
figs. 22-25
: Nicoll, 1923^: 240, 246
Hall, 1923 : 14
; Ciurea, 1924 : 14
Cram, 1926 : 43
•Pres.
Fclis cuius dom., Canis
familiaris, I'ulpcs lugopus.
Rossicotrema simile
Ciurea, 1924 ; 14, 17
•Pres.
Rossicotrema venustum
Ciurea, 1924 : 14
•Pres.
ScAPHANOCtPUALUb
ScAPHANOCEMIALUS
!
[agerskjbld, 1903 : 1-16
I.iihe, 1909 : 88, 89
Odhncr, 1914 : 244
Skrjabin, 1916 : 13
Ransom, 1920 : 527, 528
Nicoll, : 168
Ciurea, 1924 : 1,14,18
Stunkard & 11., 1924 : 6
Pochc, 1926 : 147
Faust & N., 1926 : 91
Pres.
Scuphamctphdlus
australis
Scaphanoccphulus
australis
Johnston, 1917 : 188-195, text-tigb.
1-5, figs. l,lrf
! Ciurea, 1924 : 18
Pres.
Ilaliaclus Iciuoguslcr
caphamccphulus
cxpansus
Scaphunvciphulus
cxpansus \
Jagcrskjold, 1903 ; i-iO, figs. 1-5
Liihc, 1909 : 89
Johnston, 1917 : 188, 195
Nicoll, 1923^ ; 168, 179
Ciurea, 1924 : 2, 14
Pres.
Distoma expausum
Monticelli, 1892 : 714
Monostmum expansum
Creplin, 1842 : 327 - 33 ^»
Dujardin, 1845 : 345, 346
Diesing, 1850 : 321
Brandes, 1892 : 508 |
Monticelli, 1892 ; O85, 086 , O94,
696,700,703,713,714 '
Braun, 1893 : 915
Jagcrskjold, 1901 : 979, 983
•Jagcrskjold, 1903 ; i
Pandion baluicius
Tocoirema expansum \
Jagcrskjold, 1901 : 979-981, fig. i
Looss, 1902 : 706
Odhncr, 1902 : 45 i
•Jagerskjdld, 1903 : i i
228
Valid luimc
Described as j
!
Author
Host
Stamnosoma
1
StaM NOSOMA 1
1
Tanabc, 1922 ; 19
Faust & N., 1926 : I21>122
Stiles & H., 1926 ; 93
Pres.
Sumnoiomu iirmalum
Slumnosoma armalum 1
1
i
Tanabc, 1922 : 19
Faust & N., 1926 : 93, 116, 123
Stiles & H., 1926 : 93
Nicoll, 1928 : 345, 346
Pres.
Man, Nycticorux nyctuorax^
and laboratory animals ;
metacercariac in cyprinoid
fishes.
Stdinnosom a Jormoi an u m
Stamnuwmu Jornmanum |
Nishigori, 1 924^1
Adults in man, lulis catus
;
Nishigori, 1924^
Faust & N., 1926: 93, 116, I2J,
122, 124
dom.^ Canis familiaris,
guinea-pig, rat ; mctacer-
cariae in Carassius uuratm,
i
Stiles & 11 ., 1926 : 93
Nicoll, 1928 : 345, 346
Pres.
m
Channa formosana^ Clarias
fnscus, Ctenopharyn^odott
idellus, (.'yprinus carpio,
Gambusia affinix^ Misgurtms
angiallicundatus,Opbiceph(ilus
tadianns, Paraxilnrux asolux^
Pst'udasbota parva, Rhodeux
oailutus, Zaao platypus.
Stictodora
S'lICTODOKA
Luusf', 1899 : (171 '(>72
Pratt, 1902 : 890, 910
Poche, 1926: 156
Pres.
Stictodora sazcakincnsis
1
Stictodora suivakinctuis i
1
1
1
1
Looss, 1899 : 754, 75 hg. 90
Pres.
j Larus sp.
1 Felis catus dom., (.'anis
1 familiaris, Pujinus kuhli ;
metacercariae in Mugil
1 ccpkaluSf M. capita
'I'OCOTRtMA
i
i
•'roCOTKtMA, S.Str.
I'OCOTKEMA (purtim)
i
i
Nicoll, 1909 : 483
Pres.
Looss, 1899 : 585, 586, 619
Looss, 1900 : 608
Odhncr, 1900 : 21, 22
Jagerskjold, 1900 : 736
Liihc, 19006 : 557
Braun, 1901^ : 56
Jagerskjold, 1901 : g8i, 982
Looss, 19026 : 833, 835
Jagerskjold, 1903 ; 13, 14
i
Ckvptocot\ le (partlm)
Odhncr, 1914 : 244
Skrjabin, 1919 : 13
i see Cryptocotyle (partini)
Dkrmocystis
Hallum
1
1 Stafford, 190^ ; 682
*Ran8om, 1920 : 544
Wigdor, 1918: 254
•Ransom, 1920 : 527, 547, 548
Maplcstdhe, 1922 : 1$$
Stiles Sc H*, 1926 90
229
Valid name
Described as
Author
Host
T ocotrma echinata
tocotrema echinata
Pres.
Cryptocotyle echinata
Liihe, 1909 : 88
Nicull, 1923a : 168,179
*Pre8.
Momstoma echinatum
Linstow, 1878 : 223, 224, Hg. 6
Brandcs, 1892 : 509
Monticelli, 1892: 685, 661, 694,
697, 698, 699, 702, 705, 713, 714
Braun, 1892 : 570, 586, 915
* Liihe, 1909 : 88
PanJiuit haliucius
•focotrema jejunum
'Tocotrema jejunum
Nicoll, 1907: 248, 257-259
Nicoll, 1909 : 483, figs. 20, 21
Pres.
Totunus culid/is
Cryptocotyle jejuna
Runsotii, 1920: 544, 548-550, figs.
16-17
Nicoll, 1923d : 168, 188
Ciurea, 1924 : i, 213, 18, fig. i
*Pres.
harm aigcnlatua iai-hinnutth,
iiienia hirundo.
Tocotrema lingua
Tocotrema lingua
Looss, 1899 : 586
JagcrskjoM, 1900 : 736
Jagerskjold, 1901 : 979-982
Odhner, 1902 : 45
Kowalewski, 1902 : 27 (9)
Jagerskjold, 1903 : 2, 13
Nicoll, 1906: 514,519
Nicoll, 1914 : 152
Nicoll, 1915 : 354
Pochc, 1926 : 147
Pres.
Lams a trim pill a
Larvae in Cottus not plus
Cryptocotyle americana
Ciurea, 1924: 14-15
*Prcs.
Cryptocotyle lingua
I'ischoeder, 1903 : 548
Nicoll, 1907
Liihe, 1909 : 88
Ciurea, 1915a : 446, 450
Linton, 1915: 128,134
Hissu triduciyla
Metacercuriaein various fishes
Ransom, 1920 : 544-548, figs. 12-1 s
Colymbtis auritus^ (Juvia imher^
Nvcticomx nviticoni.\, Aka
torda, Sterna dougaUi^
iS. hirundo^ Phoca viiulina.
Hall, 1923 : 14
Maplcstone, 1922 : 153-156, fig. 1
Nicoll, I9a3a : 168, 186, 190, 191,
192
Nicoll, 1923A : 2403 243, 246
Ciurea, 1924 : 14,15,18
Stunkard & IL, 1924 : 2
Poche, 1926: 148
Stunkard, 1927 : 125
•Pres.
Rattus alhuii PeU^catU) dom.
230
V'aliil name
Described as
Author
Host
'Tocolrcma litigna
Democystis ctemlabri
Stafford, 1905 : 682
Linton, 1915 : 128, 134
Distoma lingua
Crcplin, 1825 : 333, 347, 348
Creplin, 1837 = 3 *^
Dujardin, 1845 : 448
Creplin, 1846 : 139
Dicsing) 1850 : 343
Cobbold, i860 : 11
Olsson, 1876 : 15
Stossich, i892<z : 158
Braun, 1892 : 568, 599, 721
Olsson, 1893 : ii
Monticelli, 1893 : 94
Kowalewski, 1896 : 252
Stostich, 1896 : 129
1 Stossich, 1898 : 41, 42
j laihe, 1899 : 339
, Jagerskjbld, 1898 : 4, 14, lO, figs. 1-4
*Lo088, 1899: 586
; Jacoby, 1900 : 23
! Jiigcrskjdld, 1901 ; 982
Jagerskjold, 1903 : i, 5
Larus marinus
Larus ars^entatus
Larus Justus
!
Dtstoma sp.
Ryder, 1844 : 37-42
Linton, 1890 : 281, 296, figs. 76, 81
Linton, 1891 : 462, 463, fig. 318
1* Stafford, 1905 : 682
1 Linton, 1912 : 255, 257
Metacitcariae in 'Tuutogulubrus
dilaspcrsus.
j Ildllum caninum
\
Wigdor, 1918 : 254-257, figs. 1-4
•Ransom, 1920 : 527, 547, 548
Maplestonc, 1922 : 155
Hall, 1923 : 14
Canis Jumilians
1
REFERENCE LIST OF LITERATURE CONCERNING CERCARIAE OF
UNDETERMINED SPECIES OF HETEROPHYIDAE
Valid name
Described as
Author
Host
Cercaria ebromopbila
C. ebromopbila
Faust, 1922 ; 262-263, ^8-
Faust, 1924 : 292
Faust & N., 1926 : 124
Melania ohenina
C.jiavopunclata A
Kobayashi, 1922 : 12-13, ^8®* 4i 5
Blanfordia nosophora^ Pyradus
! cingulatus and different
species of Melania.
C. cor data
C, cor data
Faust, 1924: 254, 293, fig. 15
Faust & N., 1926 ; 117, 120, 124
Melanoides tubcrculatus
C, photijera
C. pbolifera
Faust, 1922 : 262, fig. 16
Faust, 1924 : 292
Faust & N., 1926 : 117, 119, 124
Viviparus polysonalus
C. transluccns
C. transluccns
Faust & N., 1926: 118, 119, 124,
fig- 23
Bytbinia strialula
C, tridonta
C. tridonta
Faust & N., 1926: 119-120, 124,
fig. 24
Bythinia sinensis
C. picta
C. picta
Faust, 1924 : 292
C.flavopunctata B
Kobayashi, 1922 : 13, figs. 6, 7
Melania liberiina^ M. reininanUi
Melania sp.
231
REFERENCE LIST OF SYNONYM A OF HETEROPHYIDEA,
Synonym
Valid name*
Anoiktostoma coleostoma
Ascoeotyle coleostomum
,, ruspidatum
Centrocestus cuspidatus
Aplorchidae ...
Heterophyioae
Api.orchtnae
IIaplorchinae
Apophu11t4s brevis
Rossieotrema donicum
,, tnajor
Apophallus muhlingi
Ascocotyle (partim) ...
Parascocotyt.e
,, italica
,, italica
,, longa
„ longa
,, minnta
,, minuta
,, nana
,, nana
,, pithecQphagicola ...
,, pithecophagicola
„ plana
Pygidiopsis genata
Ctureana
Chyptocotyee
,, cryptocotyloides
,, cryptocotyloides
„ quinqueangularis
,, quinqueangulare
C.linostomum heterophyes
Heterophyes heterophyes
C’OENOGONIMITS
nE'lKROP>rYF.S
,, Jraternus
,, heterophves
„ heterophyes ...
COF.NOGONIMIDAE
ITetf.rophyidae
COENOGONIMINAE
IIeterophyinae
Centrocesius cuspidatus vnr. eatiinus...
Cen t roees 1 us r us pidatu^
COIYTOGONIMIDAE
TIeieroptiyidae
C'dtyi.ogoniminae
1 Ietekophyinae
(.^VrYI.OC.ONTMUS
Heterophyes
„ Jraternus
,, heterophves
,, heterophyes ...
„ persicits
V
CoTYTOPITALLUS
Rossi coTREM \
,, similis
,, donicum
,, venustus
Cryptocotyle (partim) ... ... ... ....
Tocotrenta
,, americana
„ lingua
,, echinata
„ echinata
,, jejunum
,, jejunum
Distomum cahirinum ...
Ha plorch is ca h i ri n us
,, cochlear
Microlistrum cochlear
,, cochlearifortne (partim) ...
” ’’
,, cochleariforme
,, spinetum
,, cochleariforme sternae (partim)
,, cochlear
,, cochleariforme
,, coleostomum
Ascoeotyle coleostoma
„ colostomum
55 95
„ concavum
Cryptoeotyle concavum
,, cuspidatum ...
Centrocestus cuspidatus
,, diesingi
Microlistrum cochlear
,, erinaccum ...
Galaciosomum erinaceum
,, expansum
Scaphanocephalus expansus
,, fraternum (partim)
Heterophyes aequalis
,, dispar
,, heterophyes
„ hemiciclum ...
Galaciosomum lacteum
„ heteroploy es ...
Heterophyes heterophyes
,, ,, hominis
Distomum lingua (partim)
Apophallus muhlmgi
Tocotrema lingua
„ muhlingi
Apophallus muhlingi
„ sp. of Ryder, 1844
Tocotrema lingua
Dermocystm
Tocotrema
,, ctenolabri
„ lingua
•For particulars see the Reference List of Bibliography.
252
RKFERENCE LIST OF SYNONYMA OF ttE7EROPHTlDAE — continued
Synonym
Valid name*
Dirrocoelium hrtcrophyes
Heterophyes heterophyes
Ei hinostomum pyriforme
Parascocotylc italica
Fasciola hetrrophyes
Heterophyes heterophyes
(.'alarfosotnum (partim) ... ...
Microlistrum
,, cochlear
„ ' cochlear
„ cochlcariformr
„ eochleari forme
,, semifuscum
,, semifuscum
,, spinctum
„ spittrfum
Hallwm ... ... ...
Tocotrema
,, caninum
„ lingua
Haplorchidae ... ...
Heterophyidae
HArLORCIIIDINAE
Haplorchinae
IIapi.orchiinae ... ...
Ifcierophyes acgyptiacus
Heterophyes heterophyes
,, dispar limatus
,, dispar
,, clliptica ...
M etagonimus yokogawni
,, fraternus (partim) .
Heterophyes aequalis
,, dispar
, , heterophyes
„ hetrrophyes
„ nocens
Valid name (?) .
,, settfus
Heterophyes heterophyes
,, inops
,, aequalis
,, katsiiradai
, , nocens
,, pallidiis
,, heterophyes
,, persirus ...
^ let agon imus yokogawa i
,, yokogau'oi
Loossta ... ... ... ... ... ... ...*
Mei’agonimus
,, dohrooiemis
,, romanicus
,, parva
,, romanica
LnXOTUEMA
M etagonimus
,, ova turn
,, yokogawni
M rsogomtnus hetrrophyes (p.artim) ...
11 eterophyes heterophyes
,, nocens
Mrlngovimiis dobrogirnsis
Metagonimus romanicus
,, ovatus
,, yokogawai
,, parvus
,, romanicus
,, yokogawai (partim)
Metagonimus romanicus
Valid name
Mrtorchis orsophagolongus
Apophallus muhlingi
Mot^’orchitreminae ...
Haplorchintae
Mnnnstomum rxpansum ... ... ... ^..
Sea p ha nocephalus ex pa ns u s
,, lactrum
Calactosomum lactcum
,, pumilio ...
llaplorchis pumilio
,, semifuscum
Microlistrum semifuscum
Parascocotylc diminuta...
Parascocotylc minuta
Phagicola
Parascocotyi.e .
„ ' pithccophagicola ...
,, pithccophagicola
Phagicolinae ...
Centrocestinae
Rossi cotrema simile
Rossicotrema^ donicum
,, venustum
If
Stictodoridae
flETEROPHYIDAE
Tocotrema (partim) ...
Cryptocotyle (partim) Valid name
„ concavum
Crytpocotyle concavum
,, expansum...
ScaphanocephaJus expansus
T ocotrema mublingi
Apophallus muhlingi
,, yokogtitoa
Metagonimus yokogawai
Yokogawa ... ... ... ... ... ...
Metagonimus
,, yokogawa ...
„ yokogawai
*Fnr particulars ace the Reference List of Bibliography.
^33
SUMMARY
All members of Heterophyidae are reclassified on a system of
taxonomical coefficients. The family is divided into five sub-
families : Heterophyinae Ciurea, Centrocestinae Looss, Haplorchinae
Pratt, Cercarioidinae nov. subf., and Adleriinae nov. subf. Tlic
total number of genera reported is 21, of species 4^, Four new
genera are established : DiorcJiitrema, Dexiogonimus, Cercarioides,
and Adleria. Fourteen species of the family Heterophyidae are
reported from Palestinian hosts ; among these the following five
are new ones : Parascocotyle ascolonga, Cercarioides aharonii,
Adleria. minutissima, Diorchitrema pseudocirrata , and Dexiogonimus
ciureanus. A number of specific and generic names are rejected
as synonyms ; a number of species hitherto regarded as belonging
to the Heterophyidae is attributed to other systematic groups for
reasons given in the text.
I'he development of members of the Heterophyidae in the hnal
host was elucidated experimentally. It is found that, as a rule,
fish are intermediary hosts of Heterophyidae, i.e., they harbour
encysted metacercariae. The latter develop in the final host
within seven to eight days. The species of fish which serve as
secondar}^ hosts of almost all Palestinian Heterophyidae are listed.
Inter alia, 100 per cent, of mullets sold on the Palestinian markets
are infected with the metacercariae of Heterophyes species and
should be regarded as the source of human infection.
An almost full bibliography dealing with all specific, generic, etc.,
names of Heterophyidae and their synonyms is given.
For the purpose of comparison by other workers the following
species are deposited in the United States National Museum, the
Liverpool School of Tropical Medicine, the Zoological Museum
of the Berlin University, Molteno Institute, Cambridge, and
Helminthological Institute, Moscow.
Heterophyes heterophyes, from the dog.
Heterophyes heterophyes, from the cat.
Heterophyes dispar.
Heterophyes aequalis.
Dexiogonimus ciureanus.
Monorchitrema taihokui.
Monorchitrema taihui.
Stictodora sawakinensis.
Diorchitrema pseudocirrata .
Parascocotyle longa.
A dleria mintitissima .
234
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Vol. 52, pp. 103-186, Taf. 1-2.
A STUDY OF EXPERIMENTAL INFECTION
BY TREPONEMA DUTTON 1 ; .WITH A
REVIEW OF THE LITERATURE
BY
J. D. ALLAN GRAY, M,B., B.Sc., M.R.C.P.E.
{From the Bacteriology Department, Edinburgh Univenity)
{Received for publication 25 March, 1929)
INTRODUCTION
*
This paper records the results of a study of experimental infection
by Treponema duttoni. Although the relation of the organism to
Tick Fever in the human subject has for long been firmly established,
the literature regarding the experimental disease contains numerous
discrepancies among the observations made by different workers.
While some of the results obtained by the writer are in agreement
with observations already published, certain data elicited are
contrary to those of other workers and, therefore, appear of sufficient
importance to warrant their being recorded. The investigation
has also been of interest in eliciting certain special characteristics
of the strain of organism used — its varying pathogenicity for different
animals, the possible avenues of infection, the absence of demon-
strable antibodies in the serum of infected animals, the high resistance
of the organism to organic arsenicals and the persistence of forms
in the body after the apparent recovery of the host.
The strain of Treponema duttoni used was obtained from Dr, J. G.
Thomson, of the London School of Hygiene and Tropical Medicine,
and had been maintained for a considerable period in laboratory
animals.
Susceptible and Refractory Animals.
Experimental infection was produced in mice, rats, Vi young guinea-
pig and two monkeys {Macacus sinicus). Without exception all the
mice and rats inoculated developed the disease. In aU 348 mice
and 22 rats were infected. While Breinl and Kinghorn (1906) stated
that young guinea-pigs were more susceptible than adult ones, it was
241
fotind that adult animals were altogether refractory. Other observers
have found them refractory to various strains (Selwyn-Clarke, Le
Fanu and Ingram, 1923, and Novy and Knapp, 1906). The latter
were using a spirochaete which they termed Spirochaeta ohermeieri,
but which, according to Balfour (1911) and Cunningham (1925),
was more probably a strain of Treponema duttoni. They believed
that the scanty forms which they noted in the blood of one of three
guinea-pigs inoculated two days previously, were probably mere
survivals of those injected, but they examined the guinea-pigs only
for ten days — an insufficient length of time, since the incubation
period in the young guinea-pig successfully infected was sixteen
days. Guinea-pigs, however, have been found to be susceptible to a
Panama strain (Bates, Dunn and St. John, 1921), to a Russian strain
(Nicolle and Anderson, 1927) and to a Spanish strain (Nicolle and
Anderson, 1928).
Rabbits were refractory even when a large inoculum was injected
intravenously into young animals. Novy and Knapp (1906),
Toyota (1919) and Selwyn-Clarke, Le Fanu and Ingram (1923) like-
wise found them refractory, but they are stated td be susceptible to
large doses (Breinl and Kinghom), to intravenous injection with an
arsenic-resistant African strain (Prigge, 1926), to suboccipital injec-
tion (Plant, 1926), to inoculation into the cerebro-spinal fluid
(Strempel, 1928) and to Dakar strain (Mathis, 1927). The finding
by Norris, Pappenheimer and Flournoy (1906) of forms in the blood
of rabbits on the second day subsequent to inoculation but not
thereafter was possibly due to survival of those in the inoculum as
m the experiments of Novy and Knapp {v, supra).
Inoculum.
The inoculum for the various experiments varied. While the
blood of an infected animal was most often used, emulsions of
vdiious organs, such as of the spleen and brain and an emulsion
of the embryos from an infected mother were also successfully
employed.
Avenues of Infection.
Various modes df inoculation were investigated. All subcutaneous
and intraperitoneal injections into susceptible mice ^nd rats with
material containing visible spirochaetes produced the infection. In
addition it was found that infective material when rubbed into the
H3
unbroken or scarified skin of mice could produce the infection. In
one series of experiments great care was taken not to scarify tlie
skin, and the mice kept separate so as to avoid injury by fighting.
Th^ hair over the back of each mouse was clipped and a barium
sulphide depilating powder applied. Two days later blood con-
taining large numbers of spirochaetes was rubbed into the depilated
area with the gloved finger, and on four out of eight occasions
infection resulted. Two mice became infected even when methylated
spirit had been applied two minutes subsequent to the application
of tjie infected blood. In no case, however, in which ether alone
or iodine alone, or ether and then iodine had been applied subsequent
to the inoculation, did infection result. This possibly depended on
the penetration of the skin by the antiseptic. As recorded in a
previous paper, several workers, in contradistinction to the results
obtained by Werner (1924), state that infection can occur through
tlie unbroken skin, and the writer, who himself became accidentally
infected in the course of this work, believes that the organism gciined
access by this avenue (Gray, 1928). Moreover, the power of the
spirochaetes to penetrate various tissue cells which do not exhibit
any phagocytic action has been recorded by Strempel and Armuz/d
.(1927b).
Experimental infection was also produced by tlie avenue of
certain mucous membranes. When a drop of infected blood was
rubbed on to the nose of a liealthy mouse, infection resulted in
every case. Great care, of course, was taken not to injure the mucosa,
the blood being placed in the concavity of a sterile hollow-ground
shde and the animal's nose being gently rubbed into the concavity.
Four mice fed with infected blood all develoi^ed the infection -the
same result as thiit obtained by Feldt and Schott (1925) in 95 per
cent, of cases. Infection by the oral administration of relapsing
fever spirochaetes has also been produced in mice by Fraenkel (1907),
Nattan-Larrier (1909) and Werner (1924), and in monkeys by
F. P. Mackie (1907). Experiments similar to those of Ciwelessiany
(1927), were performed in which Treponema duttoni and Trypanosoma
brucei were appUed to the nasal mucosa, great care being taken to
avoid incidental injury. Both organisms were found to be able to
penetrate when applied either singly or in a mixture although,
according to Gwclessiany, the spirochaetes alone enter.
The question of the placental transmission was also investigated.
Hi
Samples of blood of the young born of three infected mothers were
examined for spirochaetes by the dark-ground method — all with
negative results. Two of the litters were born just before the
crisis terminating the first attack of each mother — when the blood
of the latter contained very numerous spirochaetes. Inoculation
of healthy mice with an emulsion of the body of a foetus belonging
to one of these litters revealed the presence of the spirochaetes, but
a foetus from the other litter was not infective. A mouse of the
third litter, although born two and a half months subsequent to the
last attack experienced by the mother, was proved by the inoculation
of healthy mice to be infected. Since the inoculation of an apparently
recovered mouse with trypanosomes sometimes causes the spirochaete
to reappear in the circulating blood (see p. 258) attempts were made
to demonstrate spirochaetes in the young born of an infected mother
by inoculating them with Trypanosoma^ hrucei. No spirochaetes,
however, were demonstrated by this method.
The fact that a mouse born of*an infected parent need not itself
be infected indicates that the placenta may, as stated by Strempel
and Armuzzi (1927a), have the power of hindering the passage of the
spirochaetes and the infection of young mice recorded above need
not, of course, have been conveyed via the placenta but during or
subsequent to birth (see Miki, 1925). Nevertheless, Breinl and
Kinghorn (1906), Nattan-Larrier (1911) and Leger and Bcdier (1922)
liave all produced evidence in favour of the possibility of the passage
of spirochaetes through the placenta.
Another fact elicited in this part of the work was that neither
pregnant rats nor mice when infected showed any tendency to abor-
tion. This observation is similar to that made by Breinl and
Kinghorn (1906) in regard to rats.
Incubation Period.
In computing the incubation period, daily examinations of the
peripheral blood were made by the dark-ground method, and the day
on which the organism was first observed was regarded as the first
day of the attack. Determined in this way, the incubation period
varied with the individual animaL-as well as with the species, the
dosage, the avenue of infection and the administration of drugs. "
245
'Fable I.
Showing the Variations in the Duration of the Incubation Period, Ai iacks and Intervals, and in the
Number and Severity of the Attacks in Mice.
I'hc figures denote the result of daily observations on the tail-blood by ihe dark-ground illumination
method, day i being the day on which inoculation was made.
0 denotes failure to observe spirochactes.
1 „ the observation of at least i spirochactc in the drop of blood examined.
2 „ the observation of at least i spirochactc in each field (magnification ~ 720).
„ the observation of at least 5 spirochactes in each field (magnification — 720).
4 „ the observation of at least 10 spirochactes in each field (magnification = 720).
5 „ the observation of at least 40 spirochactes in each field (magnification 720).
D „ death.
Day
I
3
4
5
6
7
8
9
10
■'
12
13
>4
15
.6
»7
18
»9
20
21
22
1
25
26
27
28
29
30
4
4
c
D
i
!
))
Sf
0
0
0
0
0
0
0
0
0
0
0
0
0
0
...
0
2
2
3
2
0
0
0 I
0
0
0
0
0
u
17
0
0
**
y
0
0
0
I
2
u
0
0
0
0
0
0
0
0
0
0
" 1 ^
0
0
0
0
0
0
))
38
0
0
0
I
3
4
4
3
4
I
2
3
4
4
4
0
0
i
D
1 i
...
0
0
1
3
! 4
i
1
0
0
I
2 '
0
0
0
I
0
0
1
I
I
0
3
3
0
1
0 I 0
0
0
0
0
0
0
u
76
0
0
I ^
4
3
2
0
0
0
0
0
0
0
0
0
0
0
I
1
C)
0
0
0
c
0
0
0
0
0
0
u
i '-’5
0
I
4
0
0
0
1
I
0
0
1
0
0
0
I
I
0
0
i
0
0
y 1 1
I
1
0
0
0
0
0
112
0
0
0
1
1 i
4
4
0
0
I
I
I
D
...
...
!
1 ^
;
!
'Fhe incubation period varied between i day (mouse 8o\ and 16 days (mouse 51).
'Fhe duration of the first attack varied between 2 days (mouse 17), and 12 days (mo\ise 38).
The duration of the intervals varied between 2 days (mouse 115), and ii days (mouse 76). (’Fhe
arbitrary criterion of an interval was absence of the spirochactes for two consecutive days.)
'Fhe number of attacks varied between 2 (mouse 17), and 5 (mouse 105).
'Fhe severity of the first attack varied between a maximum of i spirochactc in each field (mouse 17), and
a maximun of 40 spirochactes in each field, ending in death (mouse 80).
Death usually occurred during or immediately after the first attack (mice 38 and 80), but occasionally
took place in the second attack (mouse 112).
In mice the incubation period varied between one and sixteen
days (Table I). It tended to be shorter in young animals (cf. Feldt
and Schott, 1925), when large doses were given and when
subcutaneous and intraperitoneal inoculation was employed as
compared with infection through the nasal mucosa, alimentary
tract and especially the skin. Considerable variations were noted
between individual mice. For instance, three healthy mice of the
same weight were inoculated subcutaneously at the same time with
equal doses of the same infected blood ; the circulating blood of two
was positive on the day following the inoculation while that of the
third remained negative until the fourth day after inoculation.
246
Table II.
SUPKRINFECTION.
Mice 60 to 65, of approximately equal weights, were inoculated at the same time with equal doses
of the same infected material. On the fourth day mice 63 and’65 were again inoculated with infected
material. 7'hey experienced longer attacks and the spirochaetes were more numerous in their blood
than in mice 60-62. The latter also illustrate variations in the incubation period and in the duration
and severity of the first attack, when equal doses arc administered to animals of the same weight.
(The figures arc used as in Table I.)
Day
I
2
3
4
5
6
7
8
9
lO
Mouse 60
0
0
0
0
3
3
3
0
1
0
r 61 1
0
■
4
4
2
I
1
0
I-
0
,, 62
0
I
3
4
4
0
0
>
1
I
,5 •••
6
>
2
4 !
4
5 •
2
I
2
4
b 4
0
1
-
^ 1
5
4
-
0
I
1
2
65
0
1 0
1
1
3
A
4
5
3'
1
0 j
0
1
It weis also noticed that continued passage, especially when the
sub-inoculations were made from mice in the first attack, tended
slightly to shorten the incubation period and to enhtince the virulence
of the spirochaete for these animals — a finding similar to those of
Collier (1925) and Plant (1925). In contradistinction, however,
to the work of these observers and also of Sagel (1928) the virulence
for man was not lost or at least diminished, for the writer himself
became accidentally infected in the course of these investigations
(Gray, 1928).
Werner (1924) noted that in mice inoculated with Treponema
dulioni in blood taken from the human subject during afebrile
intervals, the incubation period was longest when the blood was taken
on the first or second day of the interval.
In rats the incubation period varied between one and nine days,
the longer jx^riods being observed when large doses of ' sulfarsenol '
were given intramuscularly or of * 914 ' intravenously (v, infra).
In the young guinea-pig which was infected, the incubation was
sixteen days.
The earliest observation of spirochaetes by the dark-ground
illumination method in the periph^l blood of the firM monkey was
two days, and of the second monkey thirteen days after inoculation.
247
It is of interest, however, to note that of the mice which were
inoculated at frequent intervals with the second monkey’s blood,
the first mouse to become infected was the one injected on the seventh
day after the inoculation of the monkey.
FEATURES OF THE DISEASE
The features of the disease produced in the various animals
varied considerably. Relapses were observed in mice, rats, and the
monkeys. In differentiating one attack from another, absence of
spirochaetes from the circulating blood for two consecutive days
as shown by the dark-ground illumination method was arbitrarily
taken as the criterion of an interval.
In mice the number of attacks noted varied between two and
five (Table I). The condition proved fatal in 19 per cent, of the
mice inoculated, but it was impossible to calculate the exact mortality
due to the spirochaetal infection owing to the presence of inter-
current disease such as moUvSe-typhoid. Most of the animals which
succumbed did so in the first attack, but occasionally death occurred
during the second or third attack. In contradistinction to the
findings of Tomioka (1924) neither the percentage of deaths was
higher nor the number of relapses greater after percutaneous than
after subcutaneous or intraperitoneal inoculation. Of the mice
which survived, one was found to harbour the organism in the
circulating blood four and a half months subsequent to the date of
inoculation. Persistence of infection of the blood in human cases
has been recorded by Ehrlich, Weichbrodt (1920), Mayer (1922), and
Werner (1924), and in a rat by Todd (1920).
Presence of the Spirochaetes in the Circulating Blood.
With the onset of the first attack in mice, the number of
spirochaetes increased fairly rapidly and after remaining at a fairly
constant high level for from four to twelve days decreased abruptly.
At the height of the first attack, often as many as fifty organisms
were present in each field of the dark-ground microscope
(magnification = 720) — a much greater number than in human blood
infected with Treponema dnttoni. Not infrequently when the
first attack of the mouse was of long duration — e.g., ten days or
248
more — there was for one or two days about the middle of the attack
a very considerable decrease in the number of organisms present in
the circulating blood (Table I).
An interval of from two to eleven days followed the first attack
(Table I). Thereafter spirochaetes reappeared in the circulating
blood. During such a remission although as judged by the dark-
ground illumination method, the blood did not contain the organisms,
it remained infective for healthy mice — a finding similar to those of
Novy and Knapp (1906), Breinl and Kinghorn (1906), Weichbrodt
(1921), Darling (1909), and Moselli (1923). The third and fourth
attacks, each of which lasted for one to three days, occurred at
intervals of one to eight days.
In contradistinction to Moczutkowsky (1882) it was found that
the number of organisms (visible in the blood) in each successive
attack became smaller. The statement of von Limbeck (1901)
that the organisms are not uniformly distributed tliroughout the
blood was confirmed for on several pccasions they were found to be
much more numerous in the heart blood than in blood taken from
the tail.
In fats, the number of attacks noted never exceeded three.
Buschke and Kro6 (1923) found ^that white rats showed illness
for weeks after inoculation and although the spirochaetes could not
be demonstrated in their blood, inoculation of tissue emulsion into
other animals, however, produced the disease. Toyota (1919) with
a Manchurian strain obtained relapses in rats only after the
204th passage and Bates, Dunn, and St. John (1921) only occasionally
obtained a relapse in rats. Selwyn-Clarke, Le Fanu and
Ingram (1923), working with a Gold Coast strain, found that while
black rats had only one attack, pouched rats had a relapse as well.
The young guinea-pig which was infected with a large amount
of mouse-blood rich in spirochaetes showed for two days fairly
numerous organisms in its circulating blood. It died on the third
day of the disease.
The monkeys were inoculated with infected mouse blood sub-
cutaneously. The spirochaetes were never numerous in the peri-
pheral blood and, as judged by the dark-ground method, were not
present for longer than a day at a time. Their numbers and certain
of the blood changes are depicted in the charts. During each of its
two attacks the first animal was irritable and its skin became dry.
The respirations were greatly increased, the alae nasi moving with
each respiration and diarrhoea was fairly severe. The temperature
and pulse were also increased. This monkey died on the thirty-
seventh day of the experiment.
A good illustration of an abortive attack as described by
Mayer (1922) and the writer (1928) is depicted in the chart between
nth and 13th December. Although no spirochaetes were observed
on these dates the temperature, pulse, respirations, white blood
count, and percentage of lymphocytes all showed distinct rises.
The second monkey did not present symptoms even on the four
occasions on which spirochaetes were observed and it eventually
survived the experiment only to succumb to pneumonia two months
later. It is noteworthy that the temperature, pulse, and respirations
were irregular, showing no constant deviations during the four
attacks. By the inoculation of healthy mice it was shown that this
monkey^s blood continued to be infective for 44 days subsequent to
inoculation : — thereafter it failed to produce the disease.
Changes in the Blood Count and Blood Picture.
Daily observations were made on the blood of both monkeys
(see charts). During the actual attacks there was a diminution in
the number of red blood corpuscles and in the haemoglobin, but with
each remission the number of red cells again rose though not quite to
the previous level. Mayer (1922) states that this rise during
convalescence is delayed if the spirochaetes persist in the blood.
While reticulocytes were numerous there was no poiklocytosis or
polychromatophilia as noted by Suldey (1920) in human cases in
Madagascar and no evidence of the aplastic type of anaemia stated
by Manson-Bahr to be especially noticeable in the African Tick Fever.
A rise in the white blood count was noted in connection with each
attack, due to a marked increase in the number of lymphocytes (see
charts). This change usually reached its maximum on the day
preceding the attack but was occasionally delayed until the day of
the attack. This is in keeping with the observation by Suldey of an.
increase of large mononuclears at the crisis but his statements as to
a leucopenia and a relative lymphocytosis during the intervals were
not confirmed. Karawacki and Krakowska (1921) state that the
250
NoTE.~Magnificat*ion of dark-ground microscope — 720.
251
relative lymphocytosis during the intervals is seen only when
a relapse is to occur. A leucocytosis during the attacks, due to an
increase in the number of polymorpho-nuclear neutrophil cells, has
been noted by many observers, e.g., Suldey, Mayer, Kartackeff (1925)
and Hoglund (1927), and Karawacki and Krakowska state that
this leucocytosis persists for some days after the crisis. It is
interesting to note that Manson and Thornton (1919) found a leuco-
cytosis in the cases in East Africa only when the temperature was
high or when some complication sucli as severe bronchitis was
present. Kartacheff’s observations of phagocytosis of the sipro-
ehaetes and the deflection of the Arneth Index to tlie left were not
confirmed. According to Mayer this change in the Arneth Index
persists if the spirochaetes remain in the blood after the febrile
period.
Several workers have noted during the febrile stages either
entire absence or unusual paucity of the eosinophil cells (Jouveau-
Dubreuil, 1919 ; Lebouef and Gambier, 1919 ; and Suldey). The
first-mentioned points out that in his cases in Western China this
aneosinophilia, which incidentally he found to be the only marked
alteration from the normal blood, is especially notewortliy owing
to the prevalence of concomitant parasitic infections of the intestine.
He also states that the number of eosinophils does not rise in the
intervals until after the final attack. Suldey 's contention, however,
that in the intervals there may be a relative eosinophilia throws
doubt on the efficacy of using this sudden rise, as suggested by
Jouveau-Dubreuil, as an aid in determining, after the fever has
fallen, whether or not the disease has come to an end.
It is worthy of note that D'Avigny working in the Soudan
epidemic of 1923 obtained results very different from the above.
He asserts that the number of polymorph cells which was slightly
below normal at the commencement of the disease, showed a pro-
gressive diminution up to the crisis, after which there was an increase
which reacted its maximum just before the relapse. This dis-
crepancy may, to some extent, be 'due to the fact that D’Avigny
was working with Singalese troops, for Van den Branden and Van
Hoof (1922) in the Congo allege that the leucocyte formula in natives
is naturally very in*egular.
Immunity and Super-Imposed Infection.
It was found impossible to re-infect mice or rats which had
recovered from the disease for varying periods up to eight months — a
result in keeping with the observations of Weichbrodt (1921), Sagel
(1928) and Bruynoghe and Dubois (1928). Kro6 {1925) too, found
tliat animals recovered from an infection with a Russian strain
were immune to the same strain until after the latter's passage
through a clean Ornithodorm moubata when re-infection became
possible. Nevertheless, by some the immunity is not considered
to be absolute, for Todd (1922) states that a patient may suffer from
the disease twice in a single winter, and Margolis (1919), Selwyn-
Clarke, Le Fanu and Ingram (1923), Nicolle and Conseil (1923),
Werner (1924), Oliver (1924), J. L. Kritschewsky and Brussin (1926)
and Plant l(i928b), have all recorded what they believe to be
re-infections at varying intervals after recovery either in the human
subject or in animals. Hermonius (1928), too, by the administration
of very large doses believes that he waS able to re-infect mice which
had recovered from an attack caused by Treponema duUoni five or
six weeks previously. Weichbrodt (1920), working with the
Hamburg and Elberfeld strains of the same organism, found that
mice developed an immunity which was specific only for the
homologous strain, and Bruynoghe and Dubois (1928) have suggested
that the diversity of opinions on the subject of immunity probably
results from the use of strains not strictly homologous.
Super-Imposed Infection. In determining that a reappear-
ance of the spirochaetes in the blood following a second inoculation
is due to a re-infection and not to a provocation of one still
persisting, J. L. Kritschewsky and Brussin (1926) emphasise the
difficulty in determining whether an animal has become entirely
free from the organisms which caused the original infection from
which the animal has apparently recovered. The discovery by Buschke
and Kroo of latent forms in the brains of such animals apparently
recovered renders this difhailty peculiarly acute. The writer,
however, has produced what he believes to be an infection super-
imposed on a mild primary infection camparable to those recorded
by Kudicke, F^ldt and Collier (1924), Steiner and Steinfejd (1926),
J. L. Kritschewski and Brussin (1926) and Prigge (igabh and 1926c).
Six mice were given simultaneously small equal doses of the same
253
infected blood. Four days later three of these mice received a
further and much heavier dose, and all — as judged by the number
of spirochaetes observed in the blood and by the unusual length
of the attack — became much more severely infected than the three
animals each of which had received only one dose (see Table II).
Similar results were obtained with Spirilhmi minus, and the writer,
believes that he himself suffered from a super-imposed infection
(Clray, 1928). It is interesting to note, too, that Strempel and
Armuzzi (1927a) found that mice inoculated intrapcritoneally became
immune to further intraperitoneal inoculation, but were often
susceptible to super-imposed infection by the subcutaneous route.
Skrum.
Jn vitro experiments have been described in a previous paper
(Gray, 1928). In contradistinction to Sawtschenko and Melkich
(1901) and Novy and Knapp (1906), the presence of antibodies was
not demonstrated in either the writer’s own serum withdrawn when
he was convalescent ; or in the sera of various animals taken at a
crisis and during attacks, intervals and convalescence. No agglutina-
tion or lysis was noted even after incubation at 37'^C. for twenty-four
hours. It was considered necessary to test the sera with at least
three generations of spirochaetes (in different animals) in view of the
work of Levaditi and Roche (1907), Jansco (1918), Kudicke and Feldt
(1924), Cunningham (1925), Brussin (1925), Brussin and Rogowa
(1927), Gori (1928) and Meleney (1928), who observed immuno-
logical differences between the spirochaetes of the first attack and of
the relapses. Failures to demonstrate antibodies in the serum of
convalescents have been recorded by Bruynoghe, De Greef and
Dubois (1927), and by Plaut (1928b), even although the latter
proved the patients to be completely immune to subsequent inocula-
tion. Passage through laboratory animals, too, evidently tends
to obliterate any serological distinctions originally demonstrable
such as differences in antigenic properties (Kudicke, Feldt and
Collier, 1924) or differences elicited by Rieckenberg’s adhesion test
ahd immunity reactions (Brussin and Schapiro, 1928). Kroo (1925),
however, managed by passage through a ' clean ’ Ornithodorus mouhata
to transform a Russian strain which had been maintained in mice
into a distinct serological strain.
254
An attempt made to distinguish between various generations
of relapsing fever spirochaetes by means of Rieckenberg’s reaction
was unsuccessful, although occasionally the adhesion phenomenon
was observed with platelets and bacteria when spirochaetes were
brought into contact with the serum of convalescent animals.
Briissin (1925 and 1926), however, states that in relapsing fever
the thrombocytobarin on which the reaction depends, develops one
or two days after the natural or therapeutically-induced crises in
mice, and he has thereby been able to differentiate strains of the
first and second attacks. I.ater, in 1927, in conjunction with
Rogowa he showed that in mice inoculated with organisms of the
second, third or fourth attacks, the spirochaetes of the first attack
were serologically distinct from those of the inoculum, but the
organisms 6f the first relapse were identical. Krantz (1926b) showed
that under the action of the specific serum or plasma, platelets and
bacteria adhered to the spirochaetes only when the latter were alive.
The results with the writer’s serunTand with certain of the animal
sera withdrawn after recovery may have been due to the diminution,
during the convalescence, of antibodies originally in the blood for
Lowenthal, who has used an agglutination reaction for diagnostic
purposes when spirochaetes cannot be demonstrated, found that the
agglutinating power of both human and animal blood was greatest
during the crisis of the attack and after the administration of spiro-
chaetical drugs. Wenyon (1926), too, considers it probable that
‘ antibodies which bring about the disappearance of the spiro-
chaetes in the blood, do not persist long enough to prevent relapse.’
Nevertheless, several of the specimens of blood tested were withdrawn
from a mouse or rat at the time of a crisis and even these failed to
produce any noticeable effect on successive generations of spiro-
chaetes in vitro. This would suggest that immunity against
re-infection does not depend upon the presence of immune substances
in the blood.
In vivo experiments were also performed. Attempts were made
to protect and cure mice with (i) ' immune' sera, (2) ' hyper-immune '
sera, and (3) 'vaccines.'
(i) 'Immune* sera. Three doses, each of 075 c.c. of the writer’s
blood withdrawn when he was conyalescent, and inoculated sub-
cutaneously into mice at intervals of from th^ee to four days, not only
failed to protect them from infection but, contrary to the results of
^55
Brienl and Kinghorn (1906), did not even prolong the incubation
periods. As with the in vitro experiments these results probably were
not due to the diminution during convalescence of any protective
substance which may have at one time been present, for blood with-
drawn from a rat or mouse at a crisis failed to protect or cure mice
from infection with the spirochaetes of various successive attacks.
It is possible, of course, that the amounts of serum used were too
small, for Sagel (1928) found that convalescent serum, to be of any
use, had to be exhibited in very large doses.
(2) iHyper-immune* sera (i.e., sera derived from rats after a varying
number of inoculations with infected blood) were tried for both the
prophylaxis and treatment of the disease in mice, but neither was
the incubation period prolonged nor the severity of the attack
moderated as recorded by Breinl and Kinghorn (1906), nor were
there attained the very favourable results obtained by Novy and
Knapp (1906) in the treatment of infections once established.
(3) ‘ Vaccines/ Samples of deftbrinated rats’ blood very rich in
spirochaetes were kept for forty days at oX. and at room temperature
and then inoculated into healthy mice. Unlike the results of Novy
and Knapp it was found that blood so treated, even when taken
early in the attack was not infective and even when obtained in the
later stages did not confer immunity to subsequent inoculation
with material known to be infected. J'he incfficacy of killed
spirochaetes to produce immunity has been demonstrated by
Reiter (1925) and Bruynoghe (1928) and Krant;^ (1920b), by means
of the Rieckenberg reaction, demonstrated the presence of an
anti-body which is not developed by the injection of dead spirochaetes
but only after actual infection.
In experiments to find the influence of dosage on tlie incubation
pexiod a number of mice were given a series of graded doses of
infected mouse-blood. Several of the mice which received
exceedingly high dilutions of the blood in citrate solution did not
become infected but, on being tested later, were all found to be still
susceptible. Reiter (1925), however; by injecting decreasing doses
of cultural forms into a series of mice arrived at a dose which did
not produce any evident infection and yet caused an immunity
comparable to that which succeeds an evident infection.
Experiments practically identical with those of Gori (1928) and
256
similar to th(jse of Jansco (1918), were also performed in an
endeavour to distinguish by immunity reactions, the spirochaetes of
the various successive attacks in any one mouse. Sub-inoculations
were made during the first, second and third attacks of a mouse
into further mice which, after recovery from the resulting infection,
were found to be completely immune not only to the spirochaetes
of the original attacks in each case as in Gori’s experiments but
also to those of the other stages of the disease.
All experiments performed in an attempt to demonstrate
Pfeiffer's reaction in mice with this strain of Treponema duttoni failed.
Two series of experiments were carried out. (i) Actively-motile
spirochaetes contained in mouse-blood were introduced into the
peritoneal' cavities of a series of mice which had become immune
through recovery from infection and, as a control experiment, a series
of healthy non-immune mice. At periods of one, two and four hours,
and then daily for six days subsequent to the inoculations, fluid
from each of tlie peritoneal cavities wSs removed by a pipette and
examined by the dark-ground illumination method. In no case
was there noted any difference between the two series of animals
except, of course, that the non-immune mice developed the disease
as shown by the presence of the spirochaetes in the blood, while the
others did not become infected.
{2) Actively-motile spirocliaetes contained in mouse-blood were
introduced into the peritoneal cavities of normal mice, some along
with i c.c. scrum of another mouse obtained at the crisis or obtained
after recovery from all attacks, and others with \ c.c, of the writer's
serum taken subsequent to his recovery from an accidental infection.
Control experiments in which no serum was introduced, were per-
formed in parallel. As before, successive samples of the peritoneal
fluid were examined by the dark-ground illumination method. No
difference was noted, however, between the two series of mice, all
the mice of both series becoming infected in this case.
Persistknck of Spirochaetes in the Tissues.
vSpirochaetes may persist in the body after the apparent recovery
of the host. Healthy mice were inoculated with the heart-blood
and emulsions of various organs of xecovered ammals* By this
method latent forms were found in the brain. Qi a mouse which had'
257
experienced its last attack thirty-eight days prior to being killed,
even although its heart-blood and other organs were negative.
This is in keeping with the work of Kroo (1926) and of Schauder
(1928) but contradictory to the assertion of Prigge (1926b and
1926c) that if spirochaetes are present in the brain they must also
necessarily be present in the circulating blood. I.atcnt forms in the
brain were first demonstrated by Buschke and Kroo (1923), the
latter worker showing in 1926 that the brain may harbour them as
long as ninety days after apparent recovery. Indeed, it has been
suggested that immunity to further infection lasts only for, and is
due to the persistence of the spirochaetes in the brain (Bruynoghe,
1928), but this has been contradicted by Prigge (1926b and 1926c).
Steiner and Steinfeld (1925), and Strempel and Armuzzi (r927a),
believe that they are not resistant to antibodies in the serum of the
same animal. These persistent forms in mice brain are said to be
more commonly found after re-infections (Hermonius, 1928), and
when the strain of infecting spirochaete has recently been isolated
from a human case, than when the organism has been maintained
for long in laboratory animals (Prigge and Rothermundt, 1928).
Steiner and Schauder (1925) have demonstrated persistent forms
in the bone marrow as well as in the brain, and believe, in contradis-
tinction to Strempel and Armuzzi (1927a), that the presence of
resistant forms is a regular phenomenon. Levaditi and Anderson
(1928) believe the persistent forms in the brain, as they are invisible
yet not filterable, to be intimately a.ssociated with the nerve cells,
and Plant (1928a) has shown that splenectomy has no effect on them.
Although several workers, including Krantz (1926), Kroo (1926),
Johannessohn (1926), Lebedjeva and Ssinjuschiva (1927) and
Schauder (1928), have demonstrated these latent forms even after
treatment with salvarsan, Johannessohn states that they are not
salvarsan-fast, and Prigge (1926b and 1926c) and Schreus and
Weisbecker (1926) assert that when sufficient and early doses of sal-
varsan are given, the spirochaetes quickly disappear from the brain
of mice.
J. L. Kritschewski (1927) found that different races of relapsing-
fever spirochaetes differ in their power to persist in the central
nervous system and claimed to have shown the existence of neurop-
tropic as distinct from somatotropic races of spirochaetes. Steiner
and Steinfeld (1927) and Plant (1928a) believe that these latent
forms never re-invade the blood-stream ' which, with its antibodies
appears to act as an impenetrable barrier/ Aznar (1926), however,
showed that the injection of Trypanosoma brucei or Trypanosoma
gamhiense into a mouse, recovered from a spirochaetal infection
live months previously, would cause a reappearance of the
spirochaetes in the blood two or three days later, and that th#
spirochaetes sometimes persisted there one or two days after
the trypanosomes had appeared in the blood. Savini (1923),
Wenyon (1927), Vincent (1927) and Bruynoghe (1928), have
obtained similar results and the writer has found that
inoculation with Trypanosoma brucei of rats and mice apparently
recovered - from infections with Treponema duttoni and Spirillum
minus may cause a reappearance of the spirochaetes in the
circulating blood in from one to four days. In over twenty mice
which had recovered from infection with Treponemd duttoni from
periods up to four and a half months- previous to the inoculation
with the trypanosomes it was found that if the last attack had
occurred more than one month before, no reappearance of the
spirochaetes was produced. In addition, the observation of
Bruynoghe (1928) was confirmed in that infection with Spirillum
minus of a mouse recovered from relapsing fever two or three months
previously will often cause the spirochaetes to reappear.
It is noteworthy that Joseph (1926) showed that in rats which
had apparently recovered from a relapsing fever infection, inoculation
with nagana trypanosomes did not clear the brain of the spirochaetes.
‘ TREATMliNT WITH ORGANIC ArSENICALS AND BlSMUTH.
The preparation of arsenic which the writer used first was
‘ sidphostab/ i.e., ‘ diaoxydiamino-arsenobenzol-sodium formalde-
hyde-bisulphite,’ as prepared by Messrs. Boots Pure Drug Co. Ltd.
This preparation was chosen as being one which could be administered
subcutaneously without pain or subsequent locaT reaction. Doses
of from 0*04 to 0*32 grams per kilo, of body weight given at intervals
of six to seven days were found to be valueless in protecting and
treating mice.
259
I'ablk hi.
Dxmonstratinc the Absence of Protective Properties of Tuehapevtic Doses or
* SuLPHOSTAB ’ rOR MiCE.
Each of the mice 206 to 21 1 was given subcutaneously a therapeutic close of the drug (in the
proportion of 0*04 gram to each kilo of body weight) every 6th or 7th day, and was inoculated with
infected blood on the 3rd day after the first dose. Mouse 21 ia was used as a control, being given
no * sulphostab.* Day i denotes the day on which the animals were inoculated with the infected
material. (The figures are used as in the previous Tables.)
Day
I
2
3
4
5
6
7
8
9
10
1 1
12
'3
14
15
Mouse 206
•
0
0
0
0
1
2
0
I
0
I
1
1
D
» 207
0
0
0
•
1
3
0
1
2
0
1
I
1
D
„ 208
0
0
0
0
0
0
2
2
0
I
I
1
I
0
0
n 209
0 i
0
0
0
0
2
1
0
I
-
0
0
0
0
,, 210
0
0
0
0 j
0
!
1
2
5 !
I
2
0
I !
0
c
1
n 211
0
0
0
0 ■
1
1
I
i ,
1
1
i
0
0
0
L)
» 2 I 1 A
0
0
0
0 i
1
•
3
5
‘ 1
0
I
0 1
0
-
0
I
Table IV.
Demonstrating the Absence of Protective Properties of Hvpertoxic Doses of
‘ Sulphostab ’ for Mice.
Each of the mice 212 to 215 was given subcutaneously a varying dose of the drug every 6th or
7th day, and was inoculated with the infected material at the same time as the first injection of the
drug. Mouse 220 was used as a control, being given no ‘ sulphostab.’ (The figures arc used as in the
previous Tables.)
Number of
Therapeutic
doses
given every
6 or 7 days
I
2
3
4
5
6
7
Da;
8
,^8
9
10
1 1
12
13
14
15
Mouse 212
i
0
0
0
0
I
2
4
.
I
0
1
3
0
0
» 213
2
0
0
0
0
I
3
2
1
1
0
0
0
0 1
I
I
i> 214
4
0
0
0
0
0
I
2
5
0 j
0 \
I
0
0 j
I
2
215
8
0
0
0
0
0
1
1 1
4
I 1
i i
•
1
CJ
2 ;
1
i
» 220
0
0
0
i 0
0
0
1
3
5
]
0 I
0
' !
0
0
' Bismostab,' a suspension of finely-divided metallic bismuth in
5 per cent, glucose solution also prepared by Messrs Boots, was
administered subcutaneously in doses equivalent by weight to that
recommended as the therapeutic dose for man and up to eight times
that amount, but was also found to be valueless for prophylaxis.
z6o
Table V.
«
Demonstrating i«t ABstNct, of Proieciixe Properties of iHiRArEinic anu Hiperioxic Doses
OI ‘ BlSMOblAH ’ GIVEN EVERY 6lH DaY, THE FlRSf DoSE BUNG GIVEN SIMULTANEOUSLY
WllU THE InoCLLAIION WITH THE InI-ECIED MaIXRIAL
\ thciapeutic dose of the drug was calculated as 3 6 gm per kilo, of body weight Mouse 225
was used as a control, being given no ‘ bismostab.* (The figures are used as m the previous Tables.)
Number of
Therapeutic
doses of
‘ bismostab *
given
every 6 th da}
Days
I
2
3
4
5
6
7
8
9
10
1 1
12
»3
14
15
16
Mouse 221 .
I
0
0
0
0
0
0
4
I
0
I
1
0
2
0
1
2
„ 222 .
2
0
0
0
0
0 !
0
3
1
I
0
0
0
I
I
0
0
» 223 .
4
0
0
0
0
0
•
4
I
0
0
I
1
I
0
0
0
„ 224 . .
8
0
0
0
0
0 j
3
I
0
0
0
0
1
1
0
„ 225 ...
0
0
0
0
0
0 1
1
0
2 1
I
1
0
0
0
0
0
0
1
0
* Sulphobtab,' in conjunction ‘ bismostab * was then tried
While amounts equal to eight times the ordinary therapeutic doses
of the two drugs when given together were in one case found to
protect, smaller amounts were of no effect, and doses equivalent
by weight to ten times the recommended amounts for man were
rapidly fatal. The margin between the efficient and the lethal doses
of the two drugs was, therefore, of the smallest.
Table VI.
Demunsiraiing lUE Protective Properties or Htpertoxic Doses ot ‘Sulpuosiab’
AND * Bismostab ’ given simultaneously every 6th Day
Mice 2 z 6 to 229 were given varying doses of the drugs, the first doses being administered
simultaneously witli the inoculation with the infected material Mouse 229, which received amounts
ttjual to 8 times the ordinary therapeutic doses, did not develop the disease, but mice 226 to 228, which
all leccived smaller doses, and the control mouse 230, which received no drug at all, all became infected
A therapeutic dose of * sulphostab ’ was calculated as 0*04 gram, and of ‘ bismostab ’ as 3 6 gram per
kilo of body weight. (T’hc figures arc used as in the previous Tables.)
Number of
'1 herapcutic doses
given every 6 days
Days
* Sulpho-
stab ’
* Bismo-
stab ’
1
2
♦
5
6
7
8
9
10
11
12
>3
H
*5
16
Mouse 226 .
1
1
0
0
0
0
0
I
2
5
1
1
2
I
3
3
I
0
227 ..
2
0
0
0
0
0
0
0
4
2
1
0
I
0
0
0
0
0
228 ..
4
4
0
0
0
0
D
2
1
I
0
0
1
2
I
I
0
»
229.
1
8
8
0
0
0
0 1
0
0
0
0
«
0
0
0
0
0
0
0
»
230..
0
0
0
0
0
0
0
1
0
l
3
1
1
1
0
0
0
1
d
26 i
Sulfarsenol was then administered to rats intramuscularly and
' 914 * intravenously in doses of from one to four centigrams per.
kilo, of body weight. Apart from the fact that the incubation
period was increased with these drugs on the average by two days
beyond the five days of the control rats, there was no noticeable
effect of the drug.
In view of the high resistance of the strain to arsenic as shown
by the above experiments with stdfarsenol, * 914 ’ and also by the
inefiicacy of intravenous injections of novarsenohillon in the case of
the writer who himself became accidently infected, any deprecatory
remark as to the therapeutic efficiency of the drugs tried would be
unwarranted. Numerous infections with arsenic resistant strains
are recorded both in humans (for references see Gray (1928)) and
in animals (J. L. Kritschewsky and Ljass (1925), Collier (1925), Plant
(1925), L. W. Kritschewsky (1926), Bruynoghe (1928), and P. Nicolle
(1928)). J. L. Kritschewsky (1927b) found considerable variations
in the susceptibility of seven different strains of relapsing-fevcr
spirochaetes to therapeutic doses of salvarsan and Krantz (1926a),
has brought forward some evidence suggesting that the action of
salvarsan is correlated with the development of antibodies so that
it is not necessarily greatest in the early stages of the infection.
SUMMARY
Various experiments on laboratory animals with a strain oi
Treponema duttoni are recorded, and the results obtained arc com-
pared with those of other workers.
Susceptible Animals. Mice, rats, a young guinea-pig and Macaci
sinici were successfully infected. Adult guinea-pigs and rabbits
proved refractory.
Avenues of Infection. Inoculation of susceptible animals with
infective material by the subcutaneous and intraperitoneal routes
always produced the infection. It was found that the spirochaete
could pass through the unbroken skin and mucuous membranes of
the nose and alimentary canal. The question of placental trans-
mission is discussed.
The incubation period for mice varied between one and sixteen
days. Factors influencing the length of the period have been
studied.
262
The Attacks. Several attacks were experienced by mice, rats and
monkeys, the greatest number of these species respectively being
five, three and four. The duration, severity and mortality of the
attacks have been studied.
The Spirochaetes. The duration of the presence, the numbers
and the distribution of the organisms in the blood have been studied.
Frequently, about the middle of a prolonged first attack in a mouse,
there was observed a marked decrease in the number of organisms
present in the circulating blood.
The Cellular Changes in the Blood, as observed in the monkeys,
took the form of (i) a progressive diminution in the number of red
cells and in the haemoglobin associated with the presence of reticu-
locytes, and (2) during each attack a leucocytosis with a marked
relative lymphocytosis.
Immunity and Serology. Mice and rats could not be re-infected,
but a second infection could be super-imposed on an exiting primary
one.
Antibodies were not demonstrated in the blood of an infected
human subject and animals either by in vitro or in vivo experiments
even when the serum was obtained at a crisis. No protective or
curative properties could be ascribed to ‘ immune ' sera, * hyper-
immune ' sera or * vaccines." The spirochaetes of the various attacks
in any one animal could not be distinguished by immunity reactions,
and efforts to demonstrate the Pfeiffer Reaction failed.
Persistent Forms. Persistent forms were demonstrated in the
brains of mice after apparent recovery even when the blood was not
infective to susceptible animals.
Inoculation of an apparently recovered mouse or rat with
Trypanosoma hrucei or Spirillum minus sometimes caused the
spirochaete to reappear in the circulating blood after it had dis-
appeared following recovery. ’
Arsenic Resistance. The strain was markedly resistant to organic
arsenicals. Arsenical preparations, either alone or. combined with
bismuth, had neither prophylactic nor therapeutic value except
in one mouse to which was administered hypertoxic and almost
lethal doses of ' sulphostab " combined with ‘ bismostab." The
only noticeable effect of the intramuscular administration of sulfar-
senol and intravenous injection of ‘ 914 " to rats was slightly to
lengthen the incubation period.
26s
The writer has pleasure in expressing his thanks to Professor T. J.
Mackie for his help and guidance throughout the experimental work,
to Dr. J. G. Thomson, of the London School of Hygiene and Tropical
Medicine, for supplying the strain of Treponema diittoni used ; and to
Messrs. Boots Pure Drug Co. Ltd., for the samples of ‘ bismostab '
and ‘ sulphostab.’
Part of the expenses for animals was defrayed by a grant from the
Moray Fund of Edinburgh University.
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THE DISTRIBUTION OF SANDFLIES
AND LEISHMANIASIS IN PALESTINE,
SYRIA AND MESOPOTAMIA
BY
S. ADLER, M.B., CtlB.
AND
O. THEODOR, Ph.D.
{Microbiological Tmtitute, Hebrew University, Jerusalem)
{Received for publication 7 March, 1929)
Plate IV and Two Maps
From May 12th, 1928, to October 20th, 1928, wc carried out a
survey of sandflies in Mesopotamia, Syria and Transjordnnia, in
relation to the distribution of Leishmaniasis in addition to the
study of sandflies in Palestine on which we have been engaged since
the summer of 1924. We concentrated particularly on localities
from which Leishmaniasis has been recorded but we also examined
districts in which Leishmaniasis is unknown. Obviously a survey
of such a large area in the space of one summer cannot be complete,
but it indicates the salient features in the distribution of the more
important species, for it includes the extremes and all gradations of
topographical and climatic variations within the large area examined.
In carrying out this work we were greatly helped by the Public
Health authorities and we have to thank Dr. Briercliffe of Jerusalem,
Dr. Blofield of Amman, Major Hallinan, Major Heggs, Dr. A. E. Mills,
Dr. Hannah Khayat and Dr. Sammi Beg of Baghdad, Colonel Causerct
and Dr. Mandour of Beyrout, Colonel Dagorn and Major Sondag
of Aleppo.
The distribution of Leishmaniasis in the countries under considera-
tion is probably wider than the literature on the subject indicates,
for with the increasing use of microscopical and cultural methods
of diagnosis new foci are being discovered.
Cutaneous Leishmaniasis apart from the large endemic centres
in Baghdad, Mosul and Aleppo is distributed irregularly throughout
the whole area examined.
269
2/0
Visceral Leishmaniasis has been recorded only from the Lebanon.
Lepine and Hitti (1927) recorded three cases, Professor Vregille of
the French University of Beyrout has observed two cases of infantile
J.eishmaniasis in Beyrout City and Professor Hinshaw, of the
American LTniversity of Beyrout, informs us that he observed one case
from Tripoli.
Cutaneous Leishmaniasis in dogs is known to occur in Baghdad
and Aleppo. Visceral canine Leishmaniasis has not yet been
recorded. Buxton (1923) who examined 156 dogs in Jerusalem,
Wenyon (1911) who examined no dogs in Baghdad, and Chadwick
and MacHattic (1927) who examined 130 dogs in Baghdad did not
find evidence of visceral Leishmaniasis.
METHOD OF WORK
Sandflies were dissected in saline and the alimentary tract
examined for Leishmania. The diagnosis was based in the case of
females on the spermathecae, pharynx and buccal cavity, in the case
of males on the external genitalia, pharynx and buccal cavity.
Jn addition preserved material was mounted and examined, care being
taken to mount every head in a horizontal position. The above
mentioned characters are the only ones which are legitimate for
the diagno.sis of specimens of the genus Phlehotomm for other
characters such as wing venation, palp and antennal formula are
subject to great variation and when used alone give rise to confusion.
Size and colour are also of no value for diagnosis for they vary
enormously in each species.
DIAGNOSIS OF SPECIES FOUND
The character of the male genitalia is insufficient for specific
diagnosis, e.g., in P. major and P. chinensis the male genitalia are
similar and the pattern of the male genitalia is the same throughout
the whole minutus group. It is probable that the male genitalia
will eventually prove to be of generic value. In our opinion sandflies
cannot be considered as belonging to one genus but should be raised
to the rank of a family, Phlehotomidae, For the purpose of this paper
we refer all sandflies to the genus Phlebotomus, for a revision is not
yet possible since most of the species are insufficiently described.
271
* Phlehotonms papaiasii Scop.
The pharynx of this species (Plate IV, fig. i) has been described
(1926) and the spermathecae (fig. 3, a) have been described and figured
by Grassi (1907) and Newstead (1911). This is the most widely
distributed and commonest species in the area examined.
Distribution and material examined.
Palestine and Transjordania : — Jerusalem : several thousand.
Jericho : several thousand. Haifa : 250. Amman : 120.
Djerash : 60. Maan : 70. Mozah : 300. Rosh Pinah : 300.
Tiberias : 120. (Males and females.)
Syria ; — Aleppo : 570 $$ (no males caught). Hellaweh : 2 Jo,
I $. Tripoli: 6 4 $ $. Batroun : 8 00, 4 ? $. Kubbah :
8 o 10 ? $. Enfe : 19 jj, 16 $ $. Beyrout : 6 9 9 , 2 3J.
Zachle : 3 7 9 9. Adder 13 oJ, 299. Bcherreh : i 9.
Bet Meri : i J, 3 9 9. Bar Elias : 36 43 9 9.
Mesopotamia: Baghdad: 528 9 9, ciVc. 100 33. Mosul: 40 9 9.
6 Basrah: 29 9 9.
Plilehotomus sergenti Parrot (1917).
Synonyms : — P. sergenti var. Newstead (1920).
P. sergenti var. alexandri Sinton (1928).
This species was first recorded from Algeria by Parrot. This
author described only the male for at that time (1917) no criteria
existed for diagnosing females of the genus Phlebotornus. Later
this species was recorded also from other localities. Sinton (1925)
described the distribution of this species.
DESCRIPTION
Female.
Size: 1*6 mm. to 3 mm.
Palp formula : i, 2, 4, 3, 5 or i, 4, 2, 3, 5 or i, (2, 4), 3, 5. Segment
5 is about as long or slightly larger than segment 2+3.
Antennae: Geniculated spines on, segments 3 to 15. Segment
3 > 4 + 5. In one specimen from Bcherreh : 3 < 4 + 5.
Pharynx (Plate IV, fig. 2 ; and fig. 2, b ) : The dentition is very
characteristic and at once distinguishes P. sergenti from P. papatasii,
P. major and P. chinensis. Posteriorly for a short distance the
teeth of the dorsal plate appear in optical section as long curved
scales. Anteriorly they appear as long curved teeth with their axis
longitudinal or slightly oblique. The real shape of the teeth in the
pharynx is very difficult to determine in mounted specimens viewed
dorsally. Their character can only be made out with certainty in
sagittal sections. It should therefore be understood that the
descriptions given in this paper refer only to the dorsal view of a
hat mounted head.
The above features were noted in one specimen from Algeria
presented by Dr. L. Parrot, of the Institut Pasteur d'Algerie, in
specimens from North China presented by Professor Patton and
Dr. Young, and in material caught in Mesopotamia and Syria.
The buccal cavity contains no armature.
Spefmathecae (fig. 3, c) : They consist of five or six segments (never
less than five). The superior segment is rounded and larger than
the others which diminish in diameter from befote backwards.
The duct widens considerably at its junction with the body of the
spermathecae. The above type of spcrmatheca was found in
specimens caught in Mesopotamia and Syria.
Male.
Size : 1-5 mm. to 3 mm.
Palps and Antennae as in the female.
Pharynx (Plate IV, fig. 3 ; and fig. 2, a) : As in many sandflies the
pharynx of the male is different from that of the female. It is
narrower and the teeth of the dorsal plate are much less developed
than in the female, sometimes being reduced so much that they appear
as a network of lines as in the female of P. papatasii. The teeth of
the lateral plates extend very far anteriorly. They point backwards
and appear very conspicuous on account of the feeble development
of the teeth on the dorsal plate. This type of pharynx was seen in
males from Algeria, Northern China, Mesopotamia, Syria and in
two males from the Caucasus presented by Professor Pavlowsky.
(These two specimens are probably P. li Popow. They will be
referred to later.)
Newstead (1920) described Phlehotomus sergenti var. on the
basis of two males caught in Amara. Newstead created this variety
on the following grounds ; the third segment of the antennae is
relatively much shorter than in P, sergenti and the distal spine bearing
m
processes of the second segment of the superior chisper arc markedly
unequal in length, the terminal process being three times as long as
the other in contrast to P. sev genii, in which the processes are equal.
The difference in the antennae noted by Newstead is unimportant
as the relative length of these organs and their segments is subject
to variations. Newstead's figures when measured show the same
relation between the third and fourth segment both in P. sergenii var.
and P. sergenii Parrot. Newstead illustrates the difference between
the genitalia of P. sergenii var. and P. sergenii in a diagram. The
figure given by Newstead for the genitalia of P. sergenii var. is
exactly similar to that given by Parrot (1917) in his original descrip-
tion of P. sergenii. The apparent differences noted by Newstead
depend purely on the position of the genitalia in mounting. We
had an opportunity of studying this point in a large number of
males caught in Baghdad. The terminal spine bearing processes
of the distal segment of the superior claspers are almost constantly
equal but mounted laterally one often appears longer than the other.
Sinton (1928) accepting Newstead's description of P. sergenii var.
created the variety of P. sergenii var. alexandri ; for reasons given
above we consider this a synonym of P. sergenii Parrot.
P. sergenii differs from P. sergenii var. mongolensis Sinton (1928)
in the following points. In the female the spemiathecae of P. sergenii
var. mongolensis consist of only four to five segments (fig. 3, d) ; as in
P. sergenii the superior segment is much wider than the others.
The superior clasper of P. sergenii is about two and a half times as
long as it is broad ; in P. sergenii var. mongolensis it is five times as
long as broad. The distal spine bearing processes of P. sergenii
when seen from above are equal in length ; those of P. sergenii var.
mongolensis are markedly unequal (fig. i, c-d) . The intromittant organ
in P. sergenii tapers uniformly, ending in a little knob, sometimes a
rudimentary hook ; in P. sergenii var. mongolensis it is much blunter
and the dorsal hook is rather strongly developed. The intromittant
organ of P. li is very similar to that of P. sergenii var. mongolensis
(fig. 4, d-e). In all other respects P. sergenii and P. sergenii var.
mongolensis are indistinguishable.
We compared P. sergenii from Algeria, Mesopotamia and Syria, with
two specimens from the Caucasus presented by Professor Pavlowsky.
The only difference noted was that the pedicle bearing a brush on the
*' I’lG. 1. Second segment of superior clasper of male of (a) Phlebotomus major ; ip) Phlebotomus
major var. fcrniciosus ; (c) Phlebotomus sergenti ; {il) Phlebotomus sergenti var. mongolcnsis. (e) and (d)
ventral view.
*75
first segment of the superior clasper was much wider than that of
P. sergenti. The broad pedicle is a constant feature for P. li Popow
(1925), and Sinton (1928) did not find intermediate forms between
P. li and P. sergenti. Until females of P. li are examined it will be
impossible to decide whether P. li is a distinct species or, as Parrot
thinks, a variety of P. sergenti.
Distribution and material exarr^ined. Baghdad : 683 $ $, 200 s rS.
Mosul:. 22,$?. Aleppo: in $9, 50 Bcherreh : i $.
Phlebotomus major, Annandale (1911).
The diagnostic characters in this species are to be found in the
spermathecae and the pharynx in the female, pharynx and external
genitalia in the male.
Pharynx (Plate IV, fig. 4) : The teeth appear in both sexes as
parallel rows of points. The lateral part of the toothed area extends
anteriorly as far as or slightly further than the median part.
Spermatheca (fig. 3, b) : The spermathecae consist of about twelve
segments and have a long thin tubular process (neck according to
Sinton) terminating in a little club-shaped thickening bearing a tuft of
hairs.
Male genitalia. The male genitalia in general outline resemble
those of P. chinensis but, as Sinton (1928) has pointed out, the
intromittant organ in P. major has a blunt rounded tip, while in
P. chinensis it bears a tubercle on its ventral side near the tip (fig. 4, b ) .
Fran 9a and Parrot (1921) considered P. perniciosus Newstead
to be a variety of P. major and named it P. major var. perniciosus.
Newstead (1911) in his original description of P. perniciosus pointed
out that the intromittant organ is bifid (fig. 4, c). An examination
of specimens from Algeria and France showed all the males to have
a bifid intromittant organ, i.e., they are P. major var. perniciosus.
The pharynx in both sexes and the spermathecae in the females are
similar to those of P. major. In P. major var. perniciosus the two
middle spines on the superior clasper are situated half way between
the proximal one and the two terminal ones ; in P. major from
Palestine and Syria the two middle spines are always situated
very near the proximal spine (fig. i, a-b).
In Syria and Palestine we found only males with an intromittant
organ characteristic of P. major. We therefore assume that P. major
var. perniciosus is absent or very rare in Syria and Palestine.
Distribution and maierial examined. Jerusalem: 5 3
Mozah : 15 9 9, 6 c?(^. Haifa : 30 9 9 , I2 Rosh Pinah : 9 9 9 ,
4 d' c?. Aleppo : i 9. Batroun : 4 d' c?, 2 9 9 . Kubbah : 5 d
299. Enfeh : i d. Bcherreh : i d, 8 9 9 . Cedar Grove : i 9 .
Beth Meri : 4 dd, ii 9 9. Bar Elias : 2 9 9 . Adde : 7 dd, 5 9 9 .
Zachle : 2 9 9 .
Phlehotomus chinensis Newstead.
Synonym ; — P. major var. chinensis Newstead (1916).
This species has until recently been considered a variety of
P. major. The authors (1928) pointed out that P. chinensis must be
considered a distinct species for the pharynx and spermathecae in
the female and the pharynx in the male are very different from
those of P. major. Sinton (1928) and Sinton and Barraud (1928)
have described and figured the essential differences between
P. chinensis and P. major. Patton and Hindle (1928) considered
P. chinensis to be a sub-species of P. major but the differences between
the important characters in the two sandflies are very striking ^nd
constant.
Female.
Size: Specimens from China and Syria 26 mm. to 3-2 mm.
Specimens from Palestine i-6 mm. to, i-8 mm.
Palps : I, 4, (2, 3), 5. In one specimen i. (2, 3, 4), 5.
Antennae : Segment 3>4H“5. 3 < 4 5 A-
Pharynx (Plate IV, figs. 5-6) : The toothed area in the pharynx
is triangular, the apex of the triangle being anterior. The teeth in
optical section appear as fine wedges. They are more numerous and
smaller than those of P. sergenti.
Spermathecae (fig. 3, e) : The spermathecae are much larger than
those of P. major. They are spindle-shaped, feebly chitinised
and the segmentation is incomplete and very faint. Anteriorly
there is a short process bearing a tuft of hairs. The ducts are very
wide and feebly chitinised.
Wings (fig. 5) : The wings show considerable variations. In
specimens from China and Syria the wing index aj^ varies
from 1*75 mm. to 2 3 mm., in specimens from Rosh Pinah in Palestine
from 13 mm. to i-6 mm.
277
Fig. 3. Spermalhccae of (a) Phlebotomus papatasii ; {b') Phlebotomus major ; (c) PhUhotomus
sergenti ; {d) Phlebotomus sergenti var. mongolensis ; (t*) Phlebotomus chinensis.
Fig. 4. Intromittant organ of {a) Phlebotomus chinensis from Syria. Dotted line indicates
P. chinensis from China, (i) Phlebotomus major ; (c) Phlebotomus major var. perniciosus ;
{d) Phlebotomus sergenti var. mongolensis ; {e) Phlebotomus sergenti.
►
Fig. 5. Wing of P, chinensis from Aleppo, showing variation in wing index. 7 'he dotted
outline of the small wing gives the size of specimens from Roah Pinah as compared to those of Aleppo.
278
Male.
Size, palps, antennae, pharynx and wings as in the female.
External genitalia : These are in general outline very similar to
those of P. major, Sinton (1928) pointed out several differences
between the genitalia of P. chinensis and P. major, namely the
presence of a tubercle on the intromittant organ of P. chinensis.
This tubercle is rather strongly developed in specimens from Aleppo,
in specimens from China it is much flatter and situated further away
from the tip (fig. 4, a).
It is probable that the specimens captured in Rosh Pinah represent
a local race for they are much smaller than those from China and
Syria. A comparison of specimens from China presented by Professor
Patton and Pr. Young, two specimens from India presented by Major
Sinton, and of thirteen specimens from S5nria with those from Rosh
Pinah showed that the former varied from 2-6 mm. to 3 2 mm. in
size, and the latter from i*6 mm. to i*8 mm. There were no inter-
mediate forms.
P. chinensis has previously been recorded from Northern China
(Newstead, Patton and Hindle, Young and Hertig), from the
Himalayas in India (Sinton, 1928) and from the Caucasus (Sinton,
1928). It therefore has a very wide distribution from Northern
China to Syria. It is probably present in other parts of the
Mediterranean basin but has been overlooked because of its superficial
resemblance to P. major.
Distribution and material examined, Aleppo : 8 $ 4 c?
Bcherreh : i $. Rosh Pinah : 8 $
The four species described above fall into Sinton's erect-haired
group. The table on page 279 shows their most important diagnostic
characters.
Phlebotomus minutus Rondani
This species has been re-described by the authors in 1927. For
comparison with other members of the minutus group described
in this paper further data are given. In Mesopotamia some females
were found which did not have a pigmented area in the buccal cavity.
The palp formula was usually i, 2, (3, 4), 5 or i, 2, 4, 3, 5, and excep-
tionally, I, 2, 3, 4, 5. The difference between 3 and 4 may be only 5//.
In the antennae segment 3 was always smaller than 4 + 5.
Table I.
Table of diagnostic characters for the four species of the erect-haired group.
P. papatasii.
P. major.
P. chinensis.
P. sergenti .
Pharynx
The teeth in optical section
appear as horizontal
scales or a network of
lines. The pharynx is
similar in both sexes.
The teeth in optical section
appear as parallel rows of
points. Pharynx similar
in both sexes.
The toothed area is
triangular, the teeth in
optical section appear as
fine wedges. Pharynx
similar in both sexes.
Female.— Posteriorly tl
teeth appear as hor
zontal scales. Anterior!
as strongly marked broa
teeth with their ax
longitudinal or slight
oblique.
Male.— N arrower tha
that of the female, teet
smaller. Laterally teel
extend further forwai
than medially.
Spermathccae
Cylindrical and containing
from eight to eleven
segments. The superior
segment is surmounted
by a tuft of hairs. The
ducts are narrow and
heavily chitinised.
1
1
Cylindrical and contain
about twelve segments.
Anteriorly there is a
long thin process with a
club-shaped termination
bearing a tuft of hairs.
The ducts are narrow
and lightly chitinised.
Spindle-shaped and much
larger than those of
P. major. Indications of
Incomplete segmenta-
tion. Anteriorly a short
process standing on a
broader ring bearing .a
tuft of hairs. The ducts
are wide and lightly
chitinised.
Consist of five or si
segments. The superic
segment is rounded. 1
is much longer and wid
than the others and h;
a short process bearir
a tuft of hairs.
Male Genitalia . . .
Second segment of superior
clasper longer than in-
ferior clasper. Three
terminal and two medial
short spines. Inter-
mediate appendage j
with two accessory
appendages.
Second segment of superior
clasper shorter than in-
ferior clasper. Three
medial and two terminal
long spines. Intro-
mittant organ with
rounded end.
i
Second segment .as in
P. major. Intromittant
organ bearing tubercle
near the tip ventrally.
!
Second segment very shoi
bearing two termin
and two medial lor
spines.
In the male genitalia the first segment of the superior clasper is
constantly more than twice as long as the second. The termination
of the intermediate appendage is blunt or club-shaped (fig. 6,/).
The intromittant organ is blunt and broad and notched dorsally near
its tip. This species is the most widely distributed and commonest
of the mimtus group.
Distribution and material examined.
Palestine Jerusalem : i. Jericho: 150. Jaffa: 60. Rosh
Pinah : 10 . Tiberias : 8. Haifa : 20. (Males and females.)
Fig. 6. Phlebotomus baghdadis, n.sp. (a) Buccal cavity of female ; (b) I%arynx of female ;
(c) Buccal fcavity of male ; (d) Spermatheca.
Intermediate appendage with intromitant organ of {e) Phlebotomus ba^hdadis ; (f) Phlebotomus
minutus ; (g) Phlebotomus africanus ; (h) Wing of P. bagbdadis showing variation of wing index.
Mosul : Id*.
Mesopotamia: — Baghdad: 70 $$, 31 dc^.
Basrah : 17 dd, 2 $
Syria : — Aleppo : 2 $ $, i d. Bcherreh : 2 $ $. Addeh : 2 ?
Bar Elias : i d, 3 ? Zachleh : i $. Batrun : 2 ? 9. Kubbah :
2 dd. Enfeh : i d, 5 9 9 .
In Baghdad specimens were frequently found feeding inside the
ears of geckoes where they remained as long as six hours.
Phlehotomus minutus var. niger
We found this variety only in Ben Shemen, Palestine, on a poultry
farm.
Phlehotomus africanus Newstead
This species has been sufficiently described. It is common in
Palestine but was not found in Syria and Mesopotamia. This sandfly
is in our opinion essentially an East African species and Palestine
represents its northern limit. We found it in material from
Stanleyville, Congo, sent by Dr. J. Schwetz. It is probably absent
from North-West Africa. Among a large collection of sandflies
from Algeria sent by Dr. L. Parrot we found only two species,
P. minutus and P. parroti. The latter species has probably been
confused with P, africanus owing to the similarity of the palp formula
in the two species.
Material examined, Jericho : 100. Jaffa : 40. Haifa : 10.
(Males and females.)
Phlehotomus palestinensis Adler and Theodor {1927)
This species is very rare. We found one female in Jericho and
three females in Baghdad.
Phlehotomus haghdadis n.sp.
This sandfly is about as com^liion in Baghdad as P. minutus. It is
unequally distributed and was found to be very common in some
parts of Baghdad and absent in others. The female feeds on geckoes
and birds.
Female.
Size : 1*7 mm. to 2 mm.
Palp formula : i, 2, (3, 4), 5.
Antennae: Segment 3=4 + 5. This distinguishes it from
P. mimUus, in which segment 3 is always smaller than 4 + 5.
3 < 12 ± 16.
Segment 4 is in the majority of the specimens exactly half as long
as 3.
, Wings {fig, 6 , h)\ The wing characters are variable, a is generally
shorter than > 9 , but in some specimens a was equal to /8, the wing
index being i. In the majority of the specimens the wing index aj^
was between 0 5 mm. and 0 75 mm. The termination of the first vein
also varied. In some specimens it covered the half length of a, in
others it was negative, a = 0-13 mm. to 0 3 mm. ^ — 0*3 tnm.
7 = 0*22 mm. to 0 33 mm. ^ — 0 22 mm. to + 0*14 mm.
Buccal cavity (fig. 6, a) : Pigmented area rather faint, roughly
triangular, , sometimes absent. The armature consists of a row of
sixteen to eighteen rather broad pointed teeth standing on an
arc concave posteriorly. The teeth in the middle are narrower
than the side ones. The appearance of the teeth depends to some
extent on the way the specimen is mounted. In preparations
where the buccal cavity has been dissected out, the long points of
the teeth are visible, in heads mounted complete they are sometimes
not evident. The plate joining the two lateral bars of the buccal
cavity shows a deep notch which is about three-quarters of a circle
with a narrow opening. The proximal border of the plate has several
blunt processes. This plate is rather heavily pigmented for some
distance beyond the notch. Sinton figures a similar but much
smaller notch in P, habu and a very shallow notch is present in
P. shorttii.
Pharynx (fig. 6, b) : The pharynx is rather narrow ; posteriorly
it is about twice as wide as anteriorly. The two side plates bear
very fine slender teeth, the dorsal plate minute short teeth.
Spermathecae (fig. 6, d) : They are similar in outline to those of
P. africanus but they are heavily #hitinised only in the superior
three-quarters of the capsule and the duct is very wide and feebly
chitinised.
Male.
Palps and antennae as in the female.
Wings : The variation mentioned in the female is still more
pronounced in the male, the wing index ajfi varying from i mm. to
0 26 mm. In one specimen, which is probably abnormal, the wing
283
index was 0 03 mm., i.e., a was thirty times as long as (fig. 6, A)
()8 = 0*0176 mm. ; a = 0 53 mm.).
Buccal cavity (fig. 6, c ) : In the female the broad plate which bears
the notch is deeply angulated and a trace of a pigmented area was
visible in some specimens. There are a few very fine pointed teeth
standing on two or three curved lines but they are only visible if the
buccal cavity is dissected out and even then appear to be absent
in some specimens.
Pharynx : The pharynx is similar in general shape to that of the
female. It has no teeth but only very faint ridges. This
distinguishes it from the pharynx of the male of P. minutus which
has many short teeth.
External genitalia : They are ver}^ similar to those of P. minutus
but show some constant differences. The first segment of the
superior clasper is nearly always exactly twice as long as the second,
while in P. minutus it is always more than twice as long. The
end of the intermediate appendages is sharply pointed ventrally
while in P. minutus the termination of this appendage is blunt or
sometimes club-shaped. The intromittant organ tapers uniformly
and has a blunt end (fig. 6, e). In P. africanus the intromittant
organ ends in a sharp point (fig. 6, g).
Diagnosis. This species is readily distinguished from P. minutus
by the pharynx, buccal cavity and spefmathecae in the female, as
well as by the third antennal segment, which is relatively longer
than in P. minutus. The male can be distinguished by the very
small teeth in the buccal cavity, antennal formula and some slight
differences in the genitalia. Systematically this species is closely
related to P. shorttii and P. habu. From P. shorttii it differs in
the shape of the notch and the teeth in the buccal cavity in both
sexes. From P. babu it differs in the number of teeth in the buccal
cavity (about thirty in P. babu) said the antennal formula.
Distribution and material examined. Baghdad : 130 $ $, 22 c^.
Basrah : i ?, 3
Types in the Microbiological Institute, Hebrew University,
Jerusalem.
^§4
PMehotomus iraqi, n.sp.
Size : 2 mm.
Palp formula : i, 2, 3, 4, 5.
Antennae : Segment 3 <4 + 5.
Wings : Index a //9 = 1. S = First vein covering half the
length of a. a = 027 mm., yS = 027 mm., 7 = 032 mm.,
h = 015 mm.
Buccal cavity (fig. 7, a) : Pigmented area absent. The teeth
(about fifty) stand on an arc convex posteriorly ; they are parallel
and have short blunt points at both ends. In front of and parallel
to the main ridge of teeth there is a second row of very small blunt
teeth.
Pharynx (fig. 7, b) : Its widest part posteriorly is four times as wide
as the narrow anterior part. It bulges out very suddenly and
narrows again. Posteriorly there are many small slender teeth
pointing backwards.
Spermathecae (fig. 7, c) : Wide tubes without any crenulation.
Similar to those of P. minutus,
Male unknown.
Diagnosis, This species is very closely related to P. squqmi-
pleuris which it resembles in every external character and in the
structure of the buccal cavity. The pharynx of P. squamipleuris
does not show the strong bulge nor the sudden narrowing in the
posterior part. The spermathecae of P. iraqi are very different
from the spine bearing spherical spermathecae of P. squamipleuris,
P. iraqi is also closely related to P. squamirostris Newstead (Syn.
P. taianensis Patton and Hindle). There are some slight differences
in the buccal cavity. The spermathecae of P. squamirostris are much
narrower than those of P. iraqi ; they have narrow ducts and show
indications of segmentation superiorly.
Material. Baghdad : i ?.
Type in the Microbiological Institute, Hebrew University,
Jerusalem.
Phlehotomus sp. near clydei Sinton.
A rather small, light coloured species.
Size : 15 mm. to i-8 mm.
Female.
Palp formula : i, 2, 4, 3, 5. *
Antennae : Segment 3 <4+5.
Wings : Index.a//S = 0 5 mm. to 0*7 mm. h usually o mm., some-
times slightly positive, a = o il mm. to 015 mm.,y8 == 0 22 mm. to
0 26 mm., 7 = 0*22 mm. to 0-28 mm., ^ = o mm. to 0*046 mm.
Buccal cavity (fig. 8, a) : Pigmented area heart-shaped, very faint.
Sixteen to seventeen teeth standing on a line very slightly convex
anteriorly. The teeth are pointed and directed towards the middle
of the buccal cavity. Behind them there is a row of small
indentations.
Pharynx (fig. 8, h) : The pharynx appears to be entirely unarmed.
Posteriorly it is less than twice as wide as anteriorly.
Spermathecae (fig. 8, e) : They are segmented and very similar to
those of P. papatasii but smaller. They have about six to eight
segments and narrow ducts which terminate separately.
Male.
Palp, Antennae, Wings as in the female.
Buccal cavity (fig. 8, c) : A row of twelve to thirteen pointed teeth,
similar in general arrangement to those of the female.
Pharynx : Narrower than in the female, otherwise similar.
External genitalia : Minutus type. The first segment of the
superior clasper is twice as long as the second. The intermediate
appendage ends in a sharply-pointed beak-like process. The
intromittant organ ends in a very sharp point (fig. ^,d).
Diagnosis. This species resembles P. clydei very closely. The
number and shape of the teeth in the buccal cavity of the male seem
to be different. Some slight differences may exist in the pharynx
which, posteriorly, is only 1*75 times as broad as anteriorly and not
three times as in P. clydei. We found no armature in the pharynx
whereas Sinton figures toothed ridges in P. clydei. In the male
genitalia the first segment of the superior clasper is exactly twice
as long as the second, while in P. clydei it is 2*3 to 2*4 times as long
as the second segment. P. clydei is a rather big species (2*2 mm. to
2*9 mm.) while the Palestinian species is only 1*5 mm. to i*8 mm.
long. The wing of P. clydei is about Three-fifths of the body length
while in our specimens it was nearly as long as the body.
Unfortunately we had no specimens of P. clydei for comparison
and cannot therefore determine the definite relationship of the
Palestinian specimens to this species.
287
Material examined, 4 2 ?? from Tiberias, Palestine.
Types in the Microbiological Institute, Hebrew University,
Jerusalem.
Key to the Species of the Minutus Group Described.
(Females only).
1. Spermathecae segmented P. near clydei
Spermathecae not segmented 2
2. Notch in posterior part of the buccal cavity P. baghdadis
No notch in posterior part of the buccal cavity 3
3. Pharynx broad and heavily toothed posteriorly 4
Pharynx slightly toothed posteriorly 5
4. Spermathecae tubular opening into a wide common duct.
Teeth in buccal cavity stand on an arc markedly convex
anteriorly P. minutus
Spermathecae capsules opening into separate ducts. Teeth
in buccal cavity stand on a straight line P. palestinensis
5. Spermathecae capsular. 40 to 50 narrow teeth in buccal
cavity standing on an arc ^slightly convex anteriorly.
Pharynx twice as wide posteriorly as anteriorly P. ajricanus
Spermathecae tubular. Teeth in buccal cavity stand on an
arc convex posteriorly. Pharynx posteriorly four times as
wide as anteriorly P, Iraqi
PARASITES OF SANDFLIES OTHER THAN LEISHMANIA
The following parasites were found : —
1. Fungi. A fungus parasitic in the coelome and in the ova was
found in P. papatasii in Palestine, and in P. papatasii and P. sergenti
in Mesopotamia and Syria. Infected eggs are completely destroyed.
This fungus has been figured by us in 1927.
2. Nematodes. Nematodes were found in the haemocoele of
P. papatasii and P. sergenti. Both eggs with morulae and active
larvae were seen and free larvae were numerous in the haemocoele.
In Baghdad two out of 683 P. sergenti and three out of 528 P. papatasii
were found infected. The nematode larvae pass from the haemocoele
into the ovary and may pass out together with the eggs. The larvae
probably invade the sandfly larvae and undergo a cycle of develop-
ment. Several laboratory bred sandflies were found infected.
3. A Criihidia of P. baghdadis. In five out of 78 $ specimens a
Crithidia was found in the midgut. In four specimens the cardia and
stomach were infected and in one specimen which showed a slight
infection only the upper part of the cardia was invaded. In the
288
cardia the flagellates were found attached to the rhabdorium by
their flagella.
Types of Parasites Found,
I. Rounded or irregular bodies without a flagellum (about 9// in
diameter) with a single nucleus and one or two blepharoplasts ; they
may have many protoplasmic vacuoles and chromatoid bodies
(fig. 9, a-c).
SOy^
Fid. 9. A Crithidia of F. baghdadis. (a-c) Rounded forms without flagellum ; (d-/>) Short
and intermediate flagellates with varying length of flagellum ; (t-l) Long forms.
2. Short and intermediate flagellates with or without a free
flagellum (lO/u to i6ju). Some of these forms were vacuolated and
contained chromatoid bodies (fig. 9, d-/i).
3. Long flagellates (up to 27/1) (fig. 9, f-/). The free part of the
flagellum may or may not be very short. These fotms were found in
the cardia. The blepharoplast is usually very close to the nucleus
which is central or slightly posterior. A slightly eosinophile flagellar
vacuole was present in all forms. The protoplasmic vacuoles when
present were often very large, sometimes larger than the nucleus.
289
The chromatoid bodies were in some specimens very numerous and
they were often much larger than the blepharoplast.
The fact that one specimen of P. baghdadis showed flagellates
in the cardia and not in the stomach and hindgut indicates that
transmission to the vertebrate host is by the bite of the insect,
although infection by ingestion or infected sandflies is also to be
expected. The vertebrate host is probably a gecko, though culture
of the heart's blood of forty-seven geckoes in Baghdad gave negative
results. Geckoes were occasionally observed eating sandflies.
Flagellates were inoculated into two scarified points on the left
forearm of a human being (9.6.28). As was to be expected the result
was negative.
4. Mites, Mites were occasionally found attached to the
abdomen of P. papaiasii and P. sergenti without apparently doing
any harm to the sandflies.
5. SpoYozoa. An oocyst of a sporozoon, probably a Hepatozoon
sp., was found in a single specimen of P. papaiasii in Jericho, in 1925.
This parasite has been previously described (1925). The result of the
inoculation of sporozoites into two human beings is still negative,
THE RELATION OF SANDFLIES OF THE ERECT-HAIRED
GROUP IN RELATION TO VISCERAL LEISHMANIASIS
In the case of Mediterranean visceral Leishmaniasis there is
unfortunately very little experimental evidence to incriminate any
particular species of Phlehotomus. The situation is further compli-
cated by the fact that the distribution of species in the Mediterranean
basin is not known with any degree of accuracy, for in all the
publications on the sandflies of this region the diagnosis of species
was based on insufficient data. In the area under discussion,
visceral Leishmaniasis is confined to the Lebanon (see Map No. i)
where the following species occur.
P. papatasii. This species occurs everywhere in this region
below the level of 1,650 metres.
P. major. This species is found in localities showing great
topographical and climatical variations. It occurs in the plain at
the foot of the Lebanon and in the hills up to a height of 2,000 metres.
We found one female in ^ house in the ancient cedar grove near
290
Bcherreh, 2,000 metres above sea level. This grove is said to be
under snow for six months in the year. P. major is relatively more
common in the mountains than in the coastal plain.
P. chinensis. This species was found in Bcherreh (1,650 metres).
It can exist within wide cUmatic ranges for it was also found in
Aleppo which has a much hotter and drier climate than the Lebanon.
P. sergenti. This species was found in Aleppo and Bcherreh.
Of the above four species the only one which has been incriminated
experimentally by feeding experiments on infected human beings
and animals as a vector of visceral Leishmaniasis is P. chinensis
(Patton and Hindle, Young and Hertig).
We have found this species in Aleppo, Bcherreh, the Lebanon
and in Rosh Pinah near Lake Tiberias, where visceral Leishmaniasis
is unknown, or is so rare that it has been overlooked.
The other three species cannot be excluded definitely as possible
carriers although their distribution does not coincide with that of the
disease. Sinton (1925) suggested P. major var. perniciosus as a
possible carrier of visceral Leishmaniasis in the Mediterranean because
it is closely related to P. argentipes but we did not find this variety
in the area examined. P. major occurs in places where the disease
is unknown, e.g., Jerusalem, Mozah near Jerusalem, Rosh Pinah,
Haifa.
P. papatasii. This species occurs in all Mediterranean foci of
visceral Leishmaniasis, but it also occurs in enormous numbers in
places where the disease is unknown, e.g., Jerusalem, Jericho,
Haifa, Jaffa, Rehoboth (all in Palestine), Baghdad, Basrah, Mosul.
The behaviour of L, infantum in the sandfly suggests that
P. papatasii may be a carrier, for the authors have shown (1927) that
cultures of a strain of L. infantum, when ingested by P. papatasii,
multiplied and adopted an anterior position. Since then several
more strains have been found to behave similarly. Further a
strain of canine visceral Leishmania presented by Professor NicoUe of
the Pasteur Institute, Tunis, produced local lesions on inoculation
into the tail of mice. Laboratory bred P. papatasii fed on these
lesions and some became infected, the flagellates tending to adopt an
anterior position. Both in the experiments with cultures and in
the direct feeding experiments on a mouse an anterior position
was only adopted vdien the resulting infection in the sandfly was
291
very heavy. In this respect L, infantum differs from L, tropica
which tends to adopt an anterior position in P. papatasii and
P. set genii even when the resulting infection is very slight. It was
also shown (1927) that the infection rate of P. papatasii with
L, infantum from cultures was diminished if the cultures were
emulsified in specific immune serum.
This is up to the present the only experimental evidence relating
Mediterranean yisceral Leishmaniasis with sandflies. It tends to
show that P. papatasii could be infected in nature only under very
favourable conditions, i.e., by feeding on a host with a large number
of parasites in the circulating blood. In the absence of direct
feeding experiments on human beings we concluded that P. papatasii
may transmit the disease but rarely.
P. sergenti. This species occurs in some foci of Mediterranean
visceral Leishmaniasis and is also present in parts free from the
disease, e.g., Baghdad, where it is very common. There is no
experimental evidence either for or against this species being a
carrier. Patton and Hindle (1928), working in China, showed
that L. donovani from experimentally infected hamsters exflagellates
in P. sergenti var. mongolensis but that the flagellates usually remain
in the stomach, very rarely ascend the cardia and never proceed
anteriorly beyond the cardia. This variety is therefore either
a very poor carrier or does not carry at all. It is uncertain whether
these observations can be applied to P. sergenti.
vSinton (1925) was the first to correlate the distribution of
Phlehotomus sp. and Leishmania sp. This method in Sinton’s hands
at once gave valuable results for it implicated P. argentipes as
the carrier of Kala-Azar and P. sergenti as the carrier of oriental
sore, but it has its limitations in the case of L. tropica and possibly
also in a case of vi.sceral Leishmaniasis. Strains of L. tropica vary
enormously in their infectivity for P. papatasii and the visceral
Leishmanias probably also vary in their infectivity for various
sandflies, e.g., cultures of several strains of Mediterranean visceral
Leishmaniasis were found to be more .infective for P. papatasii than
cultures of two strains of L. donovani from India. Further, L. donovan
bodies from cultures on immune serum exflagellated frequently in
P. papatasii in the case of the Mediterranean strains, rarely in the
case of the Indian strains (we will deal with this point more fully
292
in another communication). The differences in infectivity of
various strains of Leishmania for Phlebotomus sp. probably account
for the discrepancies between the distribution of the insect vector
and the protozoon.
Hindle (1928) showed that Chinese strains of visceral Leish-
maniasis also vary in their infectivity for sandflies and hamsters ;
the infectivity for sandflies and for hamsters are two individual
factors not necessarily correlated, for a strain may have a low
infectivity for hamsters and at the same time a very high infectivity
for sandflies and vice versa. Hindle's observations are not strictly
comparable to ours for whereas we estimated infectivity by feeding
sandflies on washed cultures Hindle fed his sandflies on infected
hamsters. ‘ Hindlegs method involves an unknown factor, namely the
influence of body juices of a vertebrate on the ingested Leishmania
for it has been shown that in P. papatasii the infection rate of a
strain of L. infantum was reduced in the presence of specific
agglutinins. Nevertheless the number of strains and the large
numbier of animals employed by Hindle in his experiments are
sufficient to prove variation in infectivity of strains both for hamsters
and sandflies. There may be other factors involved such .as
differences between races of Phlehotomm but whereas these are
hypothetical the variations in strains of Leishmania are a fact
established experimentally beyond doubt. It follows that in addition
to the valuable evidence adduced from the distribution of the
disease and various species of sandflies every focus should be examined
experimentally with regard to the behaviour of the local strains in
the local sandflies.
The distribution of visceral Leishmaniasis in the Mediterranean
basin suggests that the disease is either transmitted by a species
of insect which is common and widely distributed but is not an
efficient vector, or that it is transmitted by an efficient vector
which is comparatively rare and irregularly distributed, possibly
P. chinensis. The discovery of the latter species in a part of the
Mediterranean where visceral Leishmaniasis occurs is therefore of
great significance.
’ No further conclusions can be drawn until more sandfly surveys
of endemic foci based on modern methods of diagnosis are carried
out and correlated with feeding experiments on man and animals.
THE DISTRIBUTION OF SANDFLIES OF THE ERECT-HAIRED
GROUP IN RELATION TO ORIENTAL SORE
Foci of cutaneous Leishmaniasis are of two types.
(a) Big endemic centres such as Baghdad, where few inhabitants
escape the disease.
(b) Areas where there are a number of sporadic cases annually
but where the bulk of the population escapes the disease.
FOCI WITH SPORADIC CASES
Sporadic cases of oriental sore occur in the following places in
Palestine and Transjordania,
Jerusalem and its environments. A few endemic cases occur
annually although there are always a number of imported cases
from Persia, Baghdad and Aleppo. Dostrowsky (1926), who studied
oriental sore in Palestine, came to the conclusion that the endemic
cases in Jerusalem are not acquired through direct contact with the
imported ones.
Artuf. Oriental sore first appeared in this village in 1923.
Kantara. Kligler (1923) reported three cases from Kantara.
Jericho. This is the largest endemic focus. Oriental sore has
been known for a very long time in this town.
Amman. According to Dr. Blofield cases of oriental sore are
rather common in Amman, Djerash and the neighbouring villages.
We saw several locally acquired sores in people who never left
their village.
In Jericho P. papatasii is very common and is the only sandfly
which feeds on man. In the other above-mentioned places we
found P. papatasii and P. major. There is abundant evidence to
incriminate P. papatasii as a vector of oriental sore but P. major
has not yet been investigated experimentally. It is not present
in Jericho or in Baghdad but as previously pointed out this negative
evidence is insufficient.
In Syria sporadic cases occur in the coastal plain of the Lebanon
where P. papatasii and P. major are common. We found P. ser genii
in Bcherreh (one female) but oriental sore is unknown in this village
although we saw one imported case from Aleppo.
LARGE ENDEMIC CENTRES
Baghdad. This famous focus of oriental sore was investigated
in detail. We commenced work in Baghdad on May 13th, 1928, and
continued with two interruptions up to July 12th. The method of
work was as follows : Baghdad was divided into districts and a
number of houses were examined in each one. As many sandflies
as possible were collected in each district and taken to the Central
Laboratory where they were dissected and diagnosed. At the same
time observations were made on the prevalence of oriental sore
in each district and these observations were co-related with the
numbers and species of sandflies present. In all quarters examined
the proportion of P. sergenti to P. papatasii was determined by
dissection of <::aught females. The area examined included Baghdad,
Muadham, a small town five kilometres north of Baghdad, the
Royal Air Force Camp at Hunaidi, south of Baghdad, and the
agricultural experimental station at Rustamiyah.
The only two species which come into consideration as possible
carriers in Baghdad are P. sergenti and P. papatasii. P. major and
P. chinensis were not found.
Owing to the structure of the houses it is difficult to form a
relative quantitative estimate of sandflies in Baghdad. The houses
are built of bricks, the walls in many houses are not plastered and the
interstices in the walls form an admirable refuge for sandflies when
disturbed. On several occasions we saw large numbers of sandflies
disappear quickly into cracks in the walls after being disturbed by
moving a few chairs. An examination conducted a few minutes
later showed very few sandflies in the room. The insects are not
common in the upper stories and in rooms occupied during the day.
Most houses have a large cellar (sardab) originally intended for shelter
during the heat of the day but often used as a lumber room. During
the day sandflies seek shelter and humidity in dark cool rooms and
in the cellar inside holes in the walls where they- are extremely
difficult to find and capture. During summer the inhabitants sleep
on the roof and the sandflies after feeding enter cracks in the walls
of the courtyard where they are almost impossible to detect. Sand-
flies are common in bathrooms (hammams) which are dark, moist
and badly ventilated, and unless the cellars and bathrooms are
Z95
examined, few sandflies are seen. In modern houses with smooth
walls and without cellars sandflies are found in bedrooms and living-
rooms where they are easy to detect and capture.
The survey showed that the distribution of P. sergenti and
P. papatasii in Baghdad is very unequal.
In Haidar Khan and in the Jewish and Armenian quarters where
scarcely anyone escapes infection, P. sergeMi is the common species
and P. papatasii is so rare that it can be safely excluded as
the local carrier.
In the Senhac district where oriental sore is also very common
P. papatasii and P. sergenti are equally numerous (in some parts
P. sergenti predominates).
Three Armenian compounds in Senhac were specially examined.
In one where about fifty families lived and every child had either
oriental sore in active form or recently healed scars of the disease,
the two species were equally common. In another compound
inhabited by six families where every individual was infected, sand-
flies were very few. Only twelve females, P. papatasii, were caught
and about twenty males of the same species were seen on the walls.
(With a little practice it is easy to distinguish males of the two
species at sight owing to the fact that the male of P. sergenti has
relatively short external genitalia and the posterior part of the body
is less curved than that of P. papatasii.) In a third compound
inhabited by over one hundred families oriental sore was common,
many children were infected but a large number showed no signs of
the disease. In this compound P. papatasii was common and
P. sergenti rare.
South-east of Senhac there is a large Armenian encampment
with a population of about two thousand. There were several cases
of oriental sore among children but the disease was found to be rare.
P. papatasii was the prevalent species in this quarter and P. sergenti
was not found.
Examining this comparatively small area including Senhac and
the Armenian encampment we were struck by the curious fact of the
proximity of a district where the bulk of the population was infected
to another where the disease is rare. The Armenian Camp is about
600 metres from Senhac ; between the two there is an open area
containing no habitations. This observation is in accord with the
theory of transmission by a biting insect with a very limited range
of movement.
Bed bugs are rare in Baghdad and the only biting insect which is
common and restricted in its range is the sandfly.
In Alwayah a new district occupied by government officials
sandflies are very numerous, probably more so than in the rest of
Baghdad. In this district P. papaiasii is six times as numerous
as P. sergenti. Cases of oriental sore have not yet appeared in
Alwayah.
The Royal Air Force Camp at Hunaidi, south of Baghdad, is
heavily infested with P. papatasii. P. sergenti is very rare.
Cutaneous Leishmaniasis is absent but sandfly fever is very common.
The ar6a round the Royal Hospital is heavily infested with
P. papatasii ; P. sergenti is scarce. Cases of oriental sore are not
uncommon but they are not nearly as numerous as in Haidar Khan
or Senhac and a large number of children escape the disease.
The town of Muadham, five kilometres north of Baghdad, was
carefully examined. The whole population has either active oriental
sore or old scars of the disease. Both P. sergenti and P. papatasii
were found, the former being the commoner species.
In the thickly populated district of Baghdad West where
practically no one escapes the disease, P. sergenti and P. papatasii
are both common, the former species predominating. Proceeding
southwards along the bank of the river the proportion of P. papatasii
to P. sergenti increases until in the southernmost suburb, i.e., the
Railway Quarters, P. papatasii is very common and P. sergenti
is rare. In this district many cases of cutaneous Leishmaniasis have
occurred but many people escape the disease.
The distribution of the two species in Baghdad shows that
in the greater part of the city P. sergenti is the main carrier and that
in districts where this species predominates practically the whole
population is infected ; where P. papatasii predominates cases occur
but many people escape infection. We conclude therefore on
evidence of distribution that P. sergenti is a more suitable carrier of
the strains of L, tropica prevalent in Baghdad than P. papatasii.
This difference between the two species may depend partly on the
fact that P. sergenti feeds more readily on injured than on normal
skin and partly on the strains of L. tropica prevalent in Baghdad.
That it is not due to any racial peculiarities of the local P. papatasii
is proved by the fact that wild specimens of P. papatasii caught in
Baghdad were easily infected by feeding through membranes on a
strain of L. tropica from Palestine which had been previously
examined in Jerusalem and found to be highly infective for
P. papatasii ; again a strain of L. tropica isolated from a naturally
occurring case in Baghdad showed a low infectivity for P. papatasii
bred from wild females caught in Jerusalem and Jericho.
The peculiar local distribution of the two species in Baghdad
appears to depend on the surroundings of the houses. Wherever
houses are surrounded by gardens or plantations with a soft soil
the predominating species is P. papatasii. In districts such as
Haidar Khan where the houses are close together and there are no
gardens P. sergenti predominates. This suggests that P. papatasii
prefers to lay its eggs in soft soil in the neighbourhood of houses, while
P. sergenti prefers to lay eggs inside houses, probably in the cellars.
Mosul is another great endemic centre of oriental sore. Both
P. papatasii and P. sergenti occur, the former species being commoner
in the houses along the river bank. The time at our disposal did
not permit a survey of sandflies and oriental sore in every district
of the town (of a total of sixty-two sandflies — $ $ — caught, forty were
P. papatasii and twenty-two were P. sergenti).
It is interesting to compare conditions in Mosul and Baghdad
with those of Basrah and district where oriental sore is either absent
or rare. Sandflies which feed on man are apparently rare in Basrah.
We found only two females, P. papatasii, during four days' collecting
in Basrah town and twenty-seven females in Ashar and Makinah.
P. sergenti was not found. The minutus group is not uncommon.
In Ashar sandflies are rare throughout the greater part of the town
but they are not uncommon in a limited area about the centre of the
town. P. papatasii, P. minutus and P. haghdadis were found but
not P. sergenti. In Makinah near Basrah where P. papatasii was
found to be rather common there is little or no endemic oriental
sore. Zobeir, a small town in the desert about 15 kilometres
from Basrah, was examined. The ground is hard and dry, the
relative humidity of the air is very low and the temperature is even
higher than in Basrah. There is no local water supply and water
is brought into the town on mules from a spring several miles distant.
298
No sandflies or mosquitos were found in the town which is free from
oriental sore.
Aleppo. This endemic centre was examined between August loth
and September 12th, 1928. The examination was conducted on
similar lines to those employed in Baghdad. The following species
of sandflies were found :
P. papaiasii : 570 $ ? (males of this species which are easily
diagnosed at sight were not collected).
P. sergenti : iii$, 50c?<i.
P. major ; i $.
P. chinensis .* 8 $ 4 c?
It will be seen that P. papaiasii and P. sergenti are the common
species in Aleppo, the. former being by far the commoner. In
one district only (Bachsita) P. papaiasii and P. sergenti were found
in almost equal numbers, but the population of this district was not
more heavily infected with oriental sore than that of other districts
on the outskirts of the town, where P, papaiasii is about ten times as
common as P, sergenti.
P. major and P. chinensis are too rare to be considered as carriers
in Aleppo where the disease is very common.
Unlike Baghdad the distribution of the disease in Aleppo does
not correspond particularly to the distribution of P. sergenti. In
the absence of experimental data and on the evidence of the distribu-
tion of the two important species we conclude that both P. papaiasii
and P. sergenti carry the disease in Aleppo.
Bar Elias. This village lies in the plain between Lebanon and
Antilebanon, about 25 kilometres south-west of Baalbek. Until
six years ago oriental sore was unknown in the village. According
to the statement of the local sheikh an epidemic followed the return
of an infected villager who had resided for some time in Aleppo
where she acquired ' Aleppo button.' During the next five years
almost all the population, adults and children, acquired the disease.
During the last twelve months no more cases occurred probably
because every susceptible person had already ’beeh infected within
the previous five years. In Bar Elias sandflies are very numerous ;
only three species were found : P, papaiasii, P. major and P. minutus.
P. sergenti was not found. P. major and P. minutus were very rare
but P. papaiasii was present in enormous numbers ; P. papaiasii
299
is therefore the only possible carrier to be considered. Bar Elias is a
striking example of a heavily infested focus of oriental sore where
P, ser genii is absent. It is interesting to note that the neighbouring
villages are entirely free from oriental sore.
The curious distribution of oriental sore in relation to the two
carriers can only be explained on the ground of variations in
infectivity of different strains of L. tropica for the insect vectors.
The epidemiological evidence collected in Baghdad proves clearly
that here we are dealing with strains which are far more infective
for P. sergenti than for P. papatasii. In Bar Elias we are dealing
with strains highly infective for P. papatasii. In Aleppo there is not
complete evidence for comparing the infectivity of the local strains
in the two species, whereas in Palestine, where P. sergenti does not
occur, the distribution of the disease shows that the dominant strains
are not highly infective for P. papatasii. There are as yet few data
for comparing the infectivity for the two sandflies of strains from
places where there are sporadic cases of oriental sore. In one
case from Artuf, where P. papatasii is abundant and P. sergenti
absent, feeding experiments showed a higher infection rate in
P. sergenti than in P. papatasii (58 per cent, in P. sergenti and 16
per cent, in P. papatasii). On the whole the evidence shows that
P. sergenti is a better carrier than P. papatasii but that some strains
are transmitted very readily by P. papatasii.
Attention must be drawn to the absence of oriental sore in
localities where P. sergenti and P. papatasii occur, e.g., Alwayah
where both species are common, Haifa where P. papatasii is abundant,
Bcherreh where both species occur.
THE INFECTION RATE OF WILD SANDFLIES WITH LEISHMANIA
The determination of the infection rate with Leishmania in wild
sandflies is of value only if the distribution of the flagellates in the
sandfly is observed. The Leishmanias of man all tend to adopt an
anterior position in the sandfly. L. tarentolae also tends to adopt an
anterior position in P. papatasii whereas L. ceramodaciyli adopts
a posterior position, but if the infection is very heavy the infection
may also extend anteriorly. A further complication exists owing
to the fact that in early infections the flagellates are confined to the
300
stomach and it is therefore impossible to distinguish between
Leishmanias with an anterior and those with a posterior position.
The sandflies which feed on man also feed on animals ; thus we
caught P. papatasii and P. sergenti in large numbers in fowl sheds,
and on dissection we found them to contain nucleated red cells
corresponding in size to those of fowls. In these two important
species we also found nucleated red cells which correspond in size
to those of geckoes. P. papatasii both wild and laboratory bred
from Baghdad and Palestine fed readily on geckoes in captivity.
As in mosquitos, there are apparently differences in feeding habits
in the same species in various localities, for Knowles (1928) states
that in Calcutta P. papatasii does not feed on lizards. It is evident
that the interpretation of infection rates of Leishmania in sandflies
is difficult, particularly so as morphological characters in Leishmanias
are of limited or no specific value. All Herpetomonad flagellates
found in wild sandflies can be regarded as belonging' to the genus
Leishmania (sensu Wenyon) and not to the genus Herpetomonas, for
owing to the life-history of the sandfly infection from adult insect to
larva can only take place by means of resistant cysts capable of living
in the ground ; this is theoretically possible, but although large
numbers of wild and laboratory bred sandflies have been dissected
by different observers in various parts of the world, no cysts of
Herpetomonas have yet been observed and this in spite of the fact
that the methods adopted for breeding sandflies are ideal for the
propagation of Herpetomonas.
The problem is to determine the species of a Leishmania found
in a wild sandfly. The ideal method is to inoculate Herpetomonad
flagellates found to adopt an anterior position in a wild sandfly into
man, but this is not always practical although we adopted this
method in Jericho and Baghdad. Here again a negative result
cannot be interpreted with any degree of certainty for it may be
due to a natural immunity in the experimental volunteer, to the
flagellates not having reached the infective stage or to the fact that
the flagellate is not a Leishmania of man. On the other hand a
positive result is conclusive.
There is one important factor which we could not investigate,
namely the seasonal variation, if aiiy, in the infection rate of wild
sandflies. Endemic foci of the second type ^uch as we have in
Palestine are not favourable for such investigations for the infection
rate is very low ; but an investigation of this type carried out
systematically throughout the whole sandfly season in a big endemic
centre such as Baghdad should give valuable results. The season
in which the majority of cases of oriental sore are acquired is not
known because the incubation period varies enormously (from
two weeks to three years) and because the early stages of the disease
are often overlooked. A determination of the sea.son of maximum
infection rate in wild sandflies is necessary in order to establish the
period when the disease is most frequently transmitted in nature.
Information of this kind would also give indications for prophylaxis.
Jericho. In 1925 the infection rate in P. papatasii was
found to be about i per 1,000. Three wild sandflies were proved to
be infected with L. tropica, for inoculation of flagellates found in their
alimentary tract into three human beings produced lesions in which
L, donovan bodies were found.
Baghdad. Of 528 wild P. papatasii dissected none were
infected. Of 683 wild P. sergenti two were infected. In one specimen
from Haidar Khan there was a slight infection in the stomach and
cardia ; in another from Baghdad West the infection in stomach
and cardia was very heavy. Flagellates from the latter were
inoculated into a human being (27.5.28) with a negative result
up to date. The only sources from which P. sergenti can acquire
an infection with Leishmania in Baghdad are as far as our knowledge
goes, man, dog and geckoes. The human and the dog’s strains of
cutaneous Leishmaniasis are probably identical but conclusive
proof is still lacking.
Aleppo. No Leishmania was found among the 690 sandflies
dissected. Wenyon (1912) found a 6 per cent, infection rate among
the sandflies of Aleppo. It is interesting to note that according to
the statements of local medical practitioners oriental sore is on
the decline in Aleppo. Whereas before the war nobody escaped the
disease many of the Europeans who came to Aleppo since the war
have not become infected. Nevertheless oriental sore is exceedingly
common ; nearly all native adults show scars and very many native
children are seen with active sores.
We have to thank Dr. E. Libman of New York whose generosity
enabled us to carry out this work.
302
SUMMARY AND CONCLUSIONS
The distribution of sandflies and Leishmaniasis was studied in
Palestine, Mesopota,mia and Syria.
The diagnostic characters of the sandflies found are given.
Phlebotomus chinensis was found in Palestine and Syria.
The epidemiological in addition to experimental evidence show
that P. papatasii and P. sergenti are carriers of oriental sore.
In Baghdad P. sergenti is the main carrier of oriental sore. In
Jericho and Bar Elias P. papatasii is the only carrier, in Aleppo both
species probably transmit the disease.
There are localities free from oriental sore in which P. sergenti
and P. papatasii occur.
The peculiarities of the distribution of oriental sore depend on the
variations in infectivity of different strains of L. tropica for the
sandfly vector.
REFERENCES
Adler, S., and Theodor, O. (1925). 'I'he experimental trammission of cutaneous Leishmaniasis
to man from Phlebotomus papatasii. Ann. Prop. Med. & Parasitol.^ 19, 365-371.
(1925). A sporozoon of Phlebotomus papatasii. Ann. Prop. Med. fef Parasitol., 19,
309 ’ 3 * 3 -
(1926). Further observations on the transmission of cutaneous Leishmaniasis to
man from Phlebotomus papatasii. Ann. Prop. Med. & Parasitol.y 20, 175-194.
(1926). On the minutus group of the genus Phlebotomus in Palestine. Bull. Ent.
Res., 16, 399 - 405 -
(1927). On a collection of Phlebotomus species of the minutus group. Ann. Prop.
Med. & Parasitol., 21, 61-68.
*■ (*927)' The behaviour of cultures of Leishmania species in Phlebotomus papatasii.
Ann. Prop. Med. i£f Parasitol., 21, 111-134.
(1928). The presence of Phlebotomus chinensis in Syria. Nature, 122, 572-573.
Buxton, P. A. (1923). Canine Leishmaniasis not found in Jerusalem. Prans, Roy, Soc. Prop.
Med. ^ 212.
Chadwick, C. R., and McHattik (1927). Notes on cutaneous Leishmaniasis in dogs in Iraq. Prans.
Roy. Soc. Prop. Med. & Hyg,, SM, 422-432.
Dostrowsky, a. (1926). A study of cutaneous Leishmaniasis in Palestine. Ann. Prop. Med. and
Parasitol., 20, 385-406.
Fran9a, C., and Parrot, L. (1921). Essai de classification des Phl^botomes. Arch. Inst. Pasteur de
VAfrique du Nord, 1, 278-281.
Grassi, B. (1907). Ricerche sui Flebotomi. Mem. Soc. Ital. Science, Sciic 3 a, 14.
Hindle, E. (1928). Further observations on Chinese Kala-Azar. Proc. Roy. Soc., B., 103, 599-6191?
Klicler, I. J. (1923). Oriental sore in Palestine, with The report .»f a new endemic focus. Prans.
Roy. Soc. Prop. Med. & Hyg't IT, 334-336.
3^3
Knowles, R. (192S). An introduction to medical Protozoology. Thacker, Spink & Co., Calcutta.
Licpine, P., and Him, Y. K. (1927). Le Kala-Azar en Syrie. JL Med. Lyon, 5 (November, 1927).
Newstead, R. (191 i). The Papataci flies (Phlehotomus) of the Maltese Islands. Ann. Trap. Med. and
Parasit^., 5 , 139-186.
(*9ic>). On the genus Phlehotomus. Part IV. Bull. Ent. Res.^ 11 , 305-31 1.
Parrot, L. (1917). Sur un nouveau Phl^botome Algerien, Phlehotomus sergenti sp. nov. Bull.
Soc. Path. Exot.j 10 , 564-567.
Patton, W. S., and Hindle, E. (1927). The development of Chinese Leishmania in Phlehotomus
major var. chinensis and Phlehotomus sergenti var. Proc. Roy. Soc.^ 5 ., 101 , 369-390.
(1928). The North Chinese species of the genus Phlehotomus [Dipteraj Psychodidae).
Proc. Roy. Soc., B., 102 , 533-551-
Popow, P. P. (1926). Ueber einen neuen russischen Phlehotomus und die blsher in Russland entdeckten
Phlebotomen. Arch. Schiffs. -u. Trop.-Hyg., 30 , 240-248.
SiNTON, J. A. (1925). Notes on some Indian species of the genus Phlehotomus. Part XI : The role of
insects of the genus Phlehotomus as carriers of disease, with special reference to India. Ind.
yi. Med. Res., 12 , 701-729.
(1928}. Notes on some Indian species of the genus Phlehotomus. Part XXIII : Phlehotomus
clydei, n.sp. Ind. Jl. Med. Res., 16 , 179-186.
(1928). The synonymy of the Asiatic species of Phlehotomus. Ind. Jl. Med. Res., 16 . 297-324.
SiNTON, J. A., and Barraud, P. J. (1928). Improved methods for the identification of some species of
Phlehotomus used in experimental work. Ind. Jl. Med. Res., 16 , 3315-331.
Young, C. W., and Hertig, M. (1927). Kala-Azar transmission experiments with Chinese sandflies
{Phlehotomus). Proc. Soc. Exp. Biol. & Med., 24 , 823-825.
Wenyon, C. M. (1911). Oriental sore in Baghdad, together with observations on a gregarine in
Stegomyia fasciata, the haemogregarine of dogs and the flagellates of house flies. Parasitol., 4 ,
273-344- '
— - - (1912). Note on the occurrence of Herpetomonas in the Phlehotomus of Aleppo. Jl. Lond.
School Trop. Med. 1 „ 98.
Map I. Showing the Relative Numbers -of P. papatasii ano P. sergenti
. IN Baghdad and Surroundings.
The first figure gives the percentage of P. papatasii, the second of /*. sergenti,
e.g., 40/60 means 40% of P, papatasii and 60% of P. sergenti.
305
EXPLANATION OF PLATE TV
Pharynx of i
2
3
4
5
6
Phlehotomus papatasii (female).
Phlebotomus sergenti (female).
Phlehotomus sergenti (male) collected from two foci.
Phlehotomus major (female).
Phlehotomus chinensis (female) from Aleppo.
Phlebotomus chinensis (female) from Rosh Pinah.
Magnification : x 350.
BLOOD SUGAR IN INFECTIONS WITH
TRYPANOSOMA LEWISI
by
RICHARD W. LINTON
{Department of Bacteriology, College of Physicians and Surgeons,
Columbia University)
{Received for publication 8 April, 1929)
The purpose of the work reported here has been to study the
effect upon rat's blood sugar of infections with Trypanosoma lewisi.
In very recent years .several papers have appeared dealing with
this subject, but their chief emphasis has been upon the relation-
ship between blood sugar and fatal trypanosome infections. Hence
it seemed of interest to test the action upon the glucose level of
T, lewisi, which, as is well known, produces an infection ending in
recovery and complete disappearance of the organisms from the
animal's body.
Schern (1925) reported the results of experiments with trypan-
osomes which tended to show that as the number of organisms in
the blood increased, the amount of glucose decreased, and that the
terminal symptoms and death of the animal were due to a hypo-
glycaemia. He believes accordingly that fatal trypanosomiasis,
where death occurs with huge numbers of parasites in the blood
stream, is a ‘ sugar sickness.' In a later paper (1928) he reports
actual determinations of the blood sugar in rabbits and a horse
infected with T. equinum and concludes as before that the infection
produces a hypoglycaemia, and that death is thus only indirectly
due to the invading organisms.
Savino (1927) has reported the effect of infections with
T, equiperdum and T. equinum on the blood glucose in dogs. He
showed that the number of trypanosomes varied with the concen-
tration of glucose, being less after the injection of insulin and greater
after glucose was given intravenously. He further noted that the
spleen plays some part in this variation since after splenectomy
neither insulin nor glucose affected the number of trypanosomes.
307
30 ^
A similar result was obtained after the nerves leading to the spleen
had been severed.
Two other papers should be noted in this brief review.
Bruynoghe, Dubois, and Bourkaert (1927) confirmed Schern’s work..
I'hey used guinea-pigs and rabbits infected with T, brucei. They
do not believe that the trypanosomes consume the blood sugar
directly, but rather that the titer of the sugar is reduced by an
insulin-like substance. This substance, they believe, is formed
either immediately by the trypanosomes, or by the action of the
parasites upon the pancreas. The evidence for this conclusion
requires considerable broadening, however, before it can be con-
sidered as more than a suggestion.
von Fepyvessy (1926) studied the blood sugar of rats infected
with T, equiperdum. He discovered that the blood sugar was
lowered as the infection progressed and that if the animal were
cured by Germanin the level of the glucose returned to normal.
He believes with Schern that disturbances in sugar metabolism
play a considerable r 61 e in the pathogenic action of the trypanosomes.
TECHNIQUE
The strain of T. lewisi used in this work was kindly furnished by
Professor W. H. Taliaferro of the University of Chicago. Blood
sugar determinations were made by a new ‘ micro ’ method recently
described by Folin (1928). This method requires the use of only
i/io c.c. of blood. The blood itself was obtained by heart puncture
under light anaesthesia with iso-amyl-ethyl barbituric acid (amytal),
apprpximately 7 mg. being given per 100 gr. of rat*. The rats were
on an ordinary laboratory diet ; they were not fed on the day when
the test was made.
Three groups of animals were used : normal rats, infected rats,
and splenectomized infected rats. These gjroups will be considered
in order.
The first group consisted of thirty-six normal rats. Blood sugar
determinations upon them gave an average of 96 mg. of glucose
per 100 c.c. of blood. The mean of the observations was 98 mg.
* The effect of iso-amyl-ethyl bathituric acid upon blood sugar concentration i» still a matter of
experiment. This point does not come into consideration here, however, since this compound was
vtsed equally in all the experiments.
309
and the extremes were 6o mg. and 165 mg. Appromixately 90 per
cent, of the observations gave values between 70 mg. and 140 mg.
of glucose per 100 c.c.
The second series of experiments dealt with rats infected intra-
peritoneally with a suspension of T. lewisi in normal salt solution.
The infection was followed by making total counts daily, or on
alternate days, of the trypanosomes in the peripheral circulation.
When this number had reached its peak, as shown by the increasing
uniformity in size of the parasites, the animals were given amytal
in the peritoneal cavity and a small amount of blood withdrawn
from the heart. The results of several experiments are shown in
fable I. The last column in this table gives the blood sugar deter-
mination on the same animals taken thirty-hve to forty days after
infection, when the rats were considered to be free of the infection,
Table I.
Blood sugar determinations on rats infected with Trypanosoma Jezvisi.
Rat
number
I^ay after
infection
1 Number of
{ trypanosomes per
j c.inm. of blood
1 Blood sugar
1 in mg.
j per 100 c.c.
.
8
i
j 240,000
! 136
!
2
8
i 2 1 8,000
i *39
1
3
8
! 300,000
i 132
4
9
1 30,000 j
1 51
5
9
; 24,000 •
126
6
9
0
0
136
7
9
2,000 :
126
8
0
59,000 1
1 13
Blood sugar in
mg. per loo c.c.,
35-40 days after
infection
»42
1 12
9 ^
9
10
1 1
12
*3
14
»5
7 2,000
7 178,000
8 59,000
8 42,000
7 I 200,000
7 ' 200,000
i
6 I 248,000
117
83
117
102
78
89
95
107
J »3
1 16
130
105
87
or to have a negligible number of parasites in the blood. The
average blood sugar at the height of the infection was rii6 gm.
the mean 115 mg., and the extremes 78 mg. and 151 mg. ;No
signifidant variations from the previous determinations were found
after the infection had disappeared. [ ,
Besides the animals shown in Table I, twelve other rats were used
in this part of the work. No actual counts of trypanosomes were
made on them, but by means of stained slides it was estimated
when the infection was at its height, and the glucose then determined.
The average blood sugar in these animals was 115 mg., the mean
III mg., and the extremes 72 mg. and 154 mg. i .
The third group was composed of rats which had been splenec-
tomized, in an attempt to increase the severity of the infection. As is
well kiiown from the work of Regendanz and Kikuth (1927), the
spleen plays a large part in causing T. lewisi to cease reproduction
and thus is re.sponsible for the fact that this infection is a compara-
tively transitory one. A considerable difficulty was encountered
in this part of the work, however, in that, following splenectomy,
many of the rats developed a severe anaemia and died. This
anaemia, as Lauda (1925) and Mayer, Borchardt and Kikuth (1926)
have shown, is due to Bartonella muris. Determinations made
on rats thus infected, but without T. lewisi infections, showed,
however, that the blood sugar did not vary from the normal limits
until the agonal stage, when a hypoglycaemia developed. It was,
therefore, considered that an influence of Bartonella muris infections
on the blood sugar could be safely ruled out, especially where, as
in the case of the rats shown in Table II no symptoms of Bartonella
ihfection were present. It was necessary to consider this point,
since Noguchi (1928) has shown that some increase in Bartonella muris
follows splenectomy in rats, even where a fatal infection is not
produced.
As Table II shows, splenectomy did give rise to higher trypan-
osome counts in the peripheral blood. Not all the animals thus
treated, however, gave such high counts, individual animals
apparently vary greatly in the severity of their infections. The
average blood sugar here was 106 mg. of glucose per 100 c.c. of
blood. The mean of the observations was 107 mg. and the extremes
83 mg. and 134 mg.
Table II.
Blood sugar determinations on splencctomizcd rats, infected with Trypanosoma lewisi.
Rat number
l^ay after infection
Number of
trypanosomes
per c.mm. of blood
Blood sugar in mg.
per 100 c.c.
.
10
209,000
99
2
10
470,000
134
9
3 1 3,000
114
■
4
7
317,000
1 i >3
5
7
253,000
1 112
6
5
458,000
102
7
(>
469,000
543
8
7
311,000
90
DISCUSSION
Infections with T. lewisi do not cause abnormal changes in the
glucose content of the blood of rats. All the determinations under
these conditions fell within the normal range of variation. The
slightly higher averages for infected than for normal animals
are probably without significance as they lie well within the range
of experimental error.
As already stated, Schern and von Fenyvessy attribute a consider-
able role in trypanosome pathogenicity to the gradual lowering of
the blood sugar which these organisms cause. Since no experi-
menters have succeeded in proving the existence of a trypanosome
toxin or other antagonistic substance, it is probable that many of
the symptoms may in fact be due to a hypoglycaemia. In this
event, the absence of symptoms in T. lewisi infections would be due
to the ability of the experimental animal to maintain a constant
level of blood sugar, until the spleen gives rise to the ‘ reproduction
inhibiting ' antibody (Taliaferro), and thus ends the severe phase
of the infection.
When the results of the present paper were in manuscript, it was
found that Regendanz and Tropp (1927) had already published
findings, dealing in part with the same subject. Their results
correspond in general to those given here. They believe that death in
trypanosome infections is due to a toxin, but only literary evidence
is given for this view. The death of infected rats following splenec-
tomy they attribute to extensive proliferation of T. lewisi. This
conclusion cannot be considered established since they made no
actual trypanosome counts, nor did they take into account the
possibility of BartoneUa muris infections in these rats. In our own
work, we found that between one-third and one-half of splenec-
tomized rats died of Bartonella muris, which corresponds to the
number of rats dying in their experiments from T. lewisi. Further-
more, the terminal hypoglycsemia which they found in rats dying
presumably from T, lewisi is also present, as we have shown, in rats
dying irom Bartonella muris. In general the existence of fatal T. lewisi
infections cannot be accepted, unless the possibility of coincident
infection with the highly fatal Bartonella muris can be ruled out.
A critique of the work of Regendanz and I'ropp has recently been
published by Schern (1929).
CONCLUSION
The blood sugar of rats is not affected by infections with T. lewisi.
A hypoglycaemia develops, however, during the terminal stage
of infection with Bartonella muris, induced by splenectomy.
REFERENCES
Bri,yno<}HE, R., Dlhois, A., and Boi^rkaert (1927). T.c sucre du sanjj au coiirs des trypanosomiarcs
cxp^riincn talcs. Bull. Acad. Roy. Med. Belgique. 7, 142- 157.
VON 1'enyvessy, B. (1916). tJber die Bedeutung dcs Stoffwechscls der Parasiten fur das Wirtsticr bci
der Trypanosomcninfektlonen. Biochem. Ztschr., 173, 289-297.
Foun, O. (1928). A new blood sugar method. Jl. Biol. Chem., T 7 ., 421-429.
Lauda, E. (.192 5)- tJber die bei Ratten nach Entmilzung aiiftrctenden achweren anamischen
Zustande. ‘ Perniciose Anamic der Ratten.’ Vircb. Arch., 2Si, 529-599.
Mayer, M., Borchardt, W., and Kikuth, W. (1926). t)ber Einschlmsc der Erythrocyten bci
expcrimenteller Anamic der Ratten (Eine neite Pataaitenj^ruppe ?). Klin. Wchnschr.. 5,
559-560.
Nogucki, II. (1928). Ktiology of Oroya Fever. XI : Comparison of Bartonella bacillijormis and
Bartonella muris. Cultivation of Bacterium murium, n.sp. Jl. Fxper, Med,^ 47, 235-247,.
Regendanz, P., and Kikuth, W. (1927). Uber die Bcdcutung der Milz fiir die Bildung dcs vcrmch-
rungshindernden Reaktionsproduct (Taliaferro). Centralbl. f. Bakt. Abt, I, 103, 271-279.
and 'Propp, C. (1927). Das X’erhalten des Bliitziickers iind des i.eberglykogens
bei mit Trypanosomen infizierten Ratten. Arch, f. Schiffs.-u. Jropeu-hy^., 31, 37f^"385.
Savino, K. (1927). Relation entre le nombre dcs 'rrypanosomes et Ics variations glyccmiqucs dans
I’infcction cxp^rimcntalc par Trypanosoma cquiperdum. C.R. Soc. Biol.,, 96, 220-221.
(1927)* Fonctlon dc la rate chez Ics animanx infcctes par Ic T rypanosoma cqniniim. C.R. Soc.
Biol., 97, 1249-1250.
ScHERN, K. (1925). liber Trypanosomen. Centralbl. f. Bakt.., 96, 356-365 and 44o-4;;4.
— ~ — (192X). Uber die Stdrung des Zuckerstoffwechscls bei Trypanosomiases und Spirochatosen.
Biochem. Ztschr., 193, 264-268.
(1929). Zur Trypanosomcnarbeit von Regendanz und 'I'ropp. Ccntmlbl. j . Bakt. Abt. I.,
Ill, I3y-H3-
Volume XXI n
November 8, 1929
No. 3
ANNALS
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Director ,
Assistant Director
Research Assistants
Sierra Leone Research Laboratory
, Vacant.
. RUPERT MONTGOMERY GORDON, M.D.
. MARION WATSON, M B.
T. H. DAVEY, M.B.
E. P. HICKS, M.B.
VI
THE MARY KINGSLEY MEDAL
This medal was struck in commemoration of the work of the late
Miss Mary Kingsley in West Africa, and is conferred in recognition
of distinguished scientific achievement.
HONORARY RECIPIENTS
Her Royal Highness Princess Christian
Lord Lister
The Right Hon. Joseph Chamberlain
Prince Auguste d’Arenberg
Mrs. Pinnock
Mr. W'illiam Adamson
Professor William Carter
RECIPIENTS
/ 905 —
Colonel Sir David Bruce, K.C.B.
Geheimrath Professor Robert Koch
Dr. A. Laveran
Sir Patrick Manson, K.C.M.G.
1907 —
Professor Daniclewsky
Dr. Charles Finlay
Mr. W. M. Haffkine
Professor Golgi
Colonel Gorgas
Professor Theobald Smith
I9!0—
Sir William Macgregor, G.C.M.G.
Professor R. B'anchard
Dr. Anton Breinl
Professor Angelo Celli
Dr. C. W. Daniels
Surgeon-General Sir Alfred Keogh
Colonel W. G. King
Professor Nocht
Professor G. H. F. Nut tall
Major Leonard Rogers
Professor J. L. Todd
Surgeon-General Walter Wyman
/9/J~
Professor Fred. V. Theobald
/ 9 / 7 —
Dr. Griffith Evans
1919 —
Dr, J W. Scott Macfie
The Oswaldo Cruz Institute, Rio de
Janeiro
1920—
Major E. E. Austen, D.S.O.
Dr. A. G. Bagshawe, C.M.G.
Dr. Andrew Balfour, C.B.
Dr. A. L. G. Broden
Mrs. Chalmers, in recognition of the
work of the late Dr. A. J. Chalmers
Professor B. Grassi
Professor R. T. Leiper
Professor F. Mesnil
Dr. Edmond Sergent
Dr. C. W. Stiles
Dr. T. Zammit
1929
Dr. G. Carmichael Low
Dr. G. A. K. Marshal], C.M.G.
Professor R. Ncwstead
Dr. A. T. Stanton, C.M.G.
Professor J. W. W. Stephens
Dr. C. M. Wenyon, C.M.G., C.B.E.
VU
THE ALAN H. MILNE MEDAL
This medal was struck to commemorate the late Alan H. Milne,
C.M.G., the first Honorary Secretary of the School (1899-1917), and
is awarded twice yearly on the recommendation of the examiners
for the Diploma in Tropical Medicine.
1926 —
John McPhail Campbell
Triloki Nath Varma
1927 —
Alexander M. Gillespie
Joseph Hector Pottinger
Ragade Sanjiva Rao
1924 —
George Maclean
Frederick John Carlyle Johnstone
Bernard Langridge Davis
1925 —
Khwaja Sam ad Shah
Alfred Robert Davies Adams
Alfred J. Hawe
1928 —
Joseph Fine
1929 —
Ian Cameron Middleton
1921 —
George PhiUip Farmer Alien
1922 —
Quintin Stewart
1923 —
John Cecil Cruickshank
vui
NOTICE
The following courses of instruction are given by the Liverpool
School of Tropical Medicine each year : — •
(1) Two courses for the Diploma in Tropical Medicine,
commencing on the ist October and the 7th January.
The D.T.M. examinations are held in December and
March.
(2) Two courses for the Diploma in Tropical Hygiene,
commencing on the loth January and the 24th April.
The D.T.H. examinations are held in March and July.
(3) Two courses in Veterinary Parasitology, commencing on
1st October and the 7th January.
DIPLOMA IN TROPICAL MEDICINE
This Diploma shall be awarded only to candidates who possess
a qualification to practise Medicine recognised for this purpose by
the University, and who present satisfactory certificates of having
attended approved courses of study, and pass the prescribed
examination.
DIPLOMA IN TROPICAL HYGIENE
This Diploma can only be taken by those who have already
obtained the D.T.M.
* The course for this Diploma will not be conducted unless
at least five applications are received, and no application for
admission can be considered later than December 21st and
March 3Tst respectively.'
FEES
D.T.M. Course
D.T.H. Course
Course in Veterinary Parasitology
Each Diploma Examination
. . . Twenty Guineas
... Ten Guineas
... Fifteen Guineas
... Five Guineas
Fee for use of a School microscope' during one term ... One Guinea.
For prospectus and further information, application should be
made to the Hon. Dean, School of Tropical Medicine, University of
Liverpool.
of i
Date of
Diploma
1904
1904
1904
1904
1904
1904
1904
1904
1904
1904
1904
1904
1904
1904
1904
1904
1904
1904
1905
1905
1905
1905
1905
1905
1905
1905
1905
1905
1905
1905
1905
1906
1906
1906
1906
1906
1906
1906
1906
1906
1906
1906
1906
1906
1906
1906
1906
1906
1906
1906
1906
1906
1906
1907
1907
1907
1907
The following have obtained the Diploma in T ropical Medicine
:he University of Liverpool : —
Diploma in Tropical Medicine
Augustine, Henry Joshua
Bennett, Arthur King
Bruce, William James
Byrne, John Scott
Clayton, Thomas Morrison
Dalziel, John McEwen
Dee, Peter
Greenidge, Oliver Campbell
Hehir, Patrick
Khan, Saiduzzafor
Laurie, Robert
Maclurkin, Alfred Robert
McConnell, Robert Ernest
Nicholson, James Edward
Philipson, Nicholas
Sharman, Eric Harding
Thomson, Frank Wyville
Walker, Geor|s;e Francis Clegg
Anderson, Catherine Elmslie
Brown, Alexander
Caldwell, Thomas Cathcart
Critien, Attilio
Hooton, Alfred
Hudson, Charles TiUon
Illington, Edmund Moritz
Macfarlane, Robert Maxwell
Maddock, Edward Cecil Gordon
Moore, James Jackson
Nightingale, Samuel Shore
Radcliffe, Percy Alexander Hurst
Young, John Cameron
Adie, Joseph Rosamund
Arnold, Frank Arthur
Bate, John Brabant
Bennetts, Harold Graves
Carter, Robert Markham
Chisholm, James Alexander
Clements, Robert William
Dundas, James
Faichnie, Norman
Jeffreys, Herbert Castclman
Mackenzie, Donald Francis
Pallthorpe, Mary Elizabeth
Palmer, Harold Thornbury
Pearsc, Albert
Sarapey, Alexander William
Smithson, Arthur Ernest
Taylor, Joseph van Someron
Taylor, William Irwin
Tynan, Edward Joseph
Watson, Cecil Francis
Willcocks, Roger Durant
Williamson, George Alexander
Allan, Alexander Smith
Allwood, James Aldred
Bond, Ashton
Branch, Stanley
Date of
Diploma
1907 Collinson, Walter Julius
1907 Davey, John Bernard
1907 Donaldson, Anson Scott
1907 Fell, Matthew Henry Gregson
1907 Gann, Thomas William Francis
1907 Graham, James Drummond
1907 Iliscock, Robert Carroll
1907 Keane, Joseph Gerald
1907 Kennan, Richard Henry
1907 Kenrick, William Hamilton
1907 Le Fanu, George Ernest Hugh
1907 Mackey, Charles
1907 Maddox, Ralph Henry
1907 McCarthy, John McDonald
1907 Raikes, Cuthbert Taunton
1907 Ryan, Joseph Charles
1907 Vallance, Hugh
1908 Caverhill, Austin Mack
1908 Crawford, Gilbert Stewart
1908 Dalai, Kaikhusroo Rustomji
1908 Dansey-Browning, George
1908 Davidson, James
1908 Dickson, John Rhodes
1908 Dowdall, Arthur Melville
1908 Glover, Henry Joseph
1908 Greaves, Francis Wood
1908 Goodbody, Cecil Maurice
1908 Harrison, James Herbert Hugh
1908 Joshi, Lemuel Lucas
1908 Le Fanu, Cecil Vivian
1908 Luethgen, Carl Wilhelm Ludwig
1908 Mama, Jamshed Byramji
1908 McCay, Frederick William
1908 McLellan, Samuel Wilson
1908 Pearce, Charles Ross
1908 Schoorel, Alexander Frederik
1908 Smith, John Maegregor
1908 Stewart, George Edward
1908 Tate, Gerald William
1908 Whyte, Robert
1909 Abercrombie, Rudolph George
1909 Allin, John Richard Percy
1909 Armstrong, Edward Randolph
1909 Barrovv, Harold Percy Waller
1909 Beatty, Guy
1909 Carr- White, Percy
1909 Chevallier, Claude Lionel
1909 Clark, William Scott
1909 Cope, Ricardo
1909 Fleming, William
1909 Hanschell, Hothcr McCormick
1909 Hayward, William Davey
1909 Henry, Sydney Alexander
1909 Innes, Francis Alexander
1909 Jackson, Arthur Frame
1909- Kaka, Sorabji Manekji
1909 McCabe-Dallas, Alfred Alexander Donald
X
Date ef
Diploma
1909 Meldrum, William Percy
1909 Murphy, John Cullinan
1909 Samuel, Mysore Gnanananclaraju
1909 Shroff, Kawasjee Byramjee
1909 Thornely, Michael Harris
1909 Turkhud, Violet Ackroyd
1909 Webb, William Spinks
1909 Yen, Fu-Chun
1910 Brabazon, Edward
1910 Castellino, Louis
1910 Caulcrick, James Akilade
1910 Dowden, Richard
1910 Haigh, William Edwin
1910 Hamilton, Henry Fleming
1910 Hefferman, William St. Michael
1910 Hipwell, Abraham
1910 Homer, Jonathan
1910 Houston, William Mitchell
1910 James, William Robert Wallace
1910 Johnstone, David Patrick
1910 ICorke, Vishnu Tatyaji
1910 Macdonald, Angus Graham
1910 Macfie, John Wm. Scott
1910 Manuk, Mack Walter
1910 Murison, Cecil Charles
1910 Nanavati, Kishavlal Balabha
1910 Nauss, Ralph Welty
1910 Oakley, Philip Douglas
1910 Pratt, Ishmael Charles
1910 Sabastian, Thiruchelvam
1910 Shaw, Hugh Thomas .
1910 Sieger, Edward Louis
1910 Sousa, Pascal John de
1910 Souza, Antonio Bernardo de
1910 Waterhouse, John Howard
1910 White, Maurice Forbes
1911 Blacklock, Donald Breadalbane
1911 Brown, Frederick Forrest
1911 Chand, Diwan Jai
1911 Holmes, John Morgan
1911 levers, Charles Langley
1911 lies, Charles Cochrane
19 1 1 Ingram, Alexander
1 9 1 1 Kirkwood, Thomas
1911 Knowles, Benjamin
1911 Liddle, George Marcus Berkeley
1911 Lomas, Emanuel Kenworthy
1911 Mackarell, William Wright
1911 MacKnight, Dundas Simpson
1911 Mascarenhas, Joseph Victor
19 1 1 Murray, Ronald Roderick
1911 Oluwole, Akidiya Ladapo
1911 Rao, Koka Ahobala
191 1 Sinton, John Alexander
191 1 Tarapurvalla, Byramji Shavakshah
1 911 Taylor, John Archibald
1911 Woods, William Medlicott
1912 Aeria, Joseph Reginald
1912 Anderson, Edmund Litchfield
19x2 Borle, James
1912 Bowie, John Tait
1912 Brassey, Laurence Percival ;
Date of
Diploma
1912 Christie, David
1912 Dillon, Henry de Courcy
1912 Dunn, Lillie Eleanor
1912 Hardwicke, Charles
1912 Jagose, jamshed Rustomji
1912 Kochhar, Mela Ram
1912 McGusty, V'ictor William Tighe
1912 Milne, Arthur James
1912 Mitra, Manmatha Nath
1912 Myles, Charles Duncan
1912 Pelly, Huntly Nevins
1912 Prasad, Bindeshwari
1912 Prentice, George
1912 Ross, Frank
1912 Russell, Alexander James Hutchison
1912 Ruthven, Morton Wood
1912 Sandilands, John
1912 Seddon, Harold
1912 Smalley, James
1912 Strickland, Percy Charles Hutchison
1912 Watson, W'illiam Russel
1913 Austin, Charles Miller
1913 Banker, Shlavux Sorabjl
1913 Becker, Johann Gerhardus
1913 Carrasco, Milton
1913 ('lark, James McKllllcan
1913 I'orsyth, Charles
1913 Grahamc, Alalcolm Claude Russell
1913 Grieve, Kclburne King
1913 Hargreaves, Alfred Ridley
1913 Hepper, Evelyn Charles
1913 I liranand, Pandit
1913 Jackson, Oswald Egbert
1913 Khaw, Ignatius Go Kek
1913 MacKelvie, Maxwell
1913 MacKinnon, John MacPhall
1913 Macmillan, Robert James Alan
1913 Mouat-Biggs, Charles Edward Forbes
1913 Noronha, John Carmel
1913 O’C.'onnor, Edward
1913 Oluboml-Becklcy, Emanuel
1913 Pestonji, Ardeshir Beliramshah
1913 Puttanna, Dodballapur Sivappa
1913 Reford, John Hope
1913 Smith, Edward Arthur
1913 Stewart, Samuel Dudley
1913 Walker, Frederick Dcarden
1913 Wilbe, Ernest Edward
1913 Wilson, Hubert Francis
1913 Yin, U!g Ba
1913 Young, William Alexander
1914 ArcullI, Hassan el
1914 Chohan, Noormahomed Kasembha
1914 Connell, Harry Bertram
1914 Gcrrard, Herbert Shaw
1914 Gimi, Hirji Dorabji
1914 Gwynne, Joseph Robert
1914 Hodkinson, Samuel Paterson
1914 Jackson, Arthur Ivan
1914 Kaushash, Ram Chander
1914 Kelsall, Charles
1914 Luanco y Cuenca, Maximino
1914 Misbah, Abdul-Ghani Naguib
XI
Date of
Diploma
1914 Naidu, Bangalore Pasupulati Balakrishna
19J4 Rowe, John Joseph Stephen
1914 Roy, Raghu Nath
1914 Shiveahwarkar, Ramchandra Vishnu
1914 Sur, Sachindra Nath
1914 Talati, Dadabhai Cursedji
1914 Wilkinson, Arthur Geden
1914 Wright, Ernest Jenner
1915 Lobo, John Francis
1915 Madhok, Gopal Dass
1915 Pearson, George Howorth
1915 Swami, K-arumuri Virabhadra
1915 Wood, John
1916 Barseghian, Mesroob
1916 Chaliha, Lakshmi Prasad
1916 Lim, Albert Liat Juay
1916 Lim, Harold Liat Hin
1916 Metzger, George Nathaniel
1916 ShdcrstrSm, Erik Daniel
1916 Wheeler, Louis
1917 Chapman, Herbert, Owen
1917 Krishnamoorthy, Yedatore Venkoba
1917 Lipkin, Isaac Jacob
1918 Watts, Rattan Claud
1919 Bowle-Evans, Charles Harford
1919 Burnie, Robert McColl
1919 Celestin, Louis Abel
1919 Cummings, Eustace Henry Taylor
1919 Darling, Georgina Renington
1919 Drake, Joan Margaret Fraser
1919 Fraser, William James
1919 Gordon, Rupert Montgomery
1919 Krige, Christian Frederick
1919 Maplcstone, Philip Alan
1919 Oluwole, Isaac Ladipo
1919 Rustomjee, Khusshuyee Jamesidjee
1919 Sawers, William Campbell
1919 Thompson, Mary Georgina
1919 Turner, Gladys Maude
1919 Young, Charles James
1920 Adler, Saul
1920 Anderson, William Jenkins Webb
1920 Campbell, George
1920 Cobb, Charles Eric
1920 Cobb, Enid Margaret Mary
1920 Connolly, Evelyn Mary
1920 Fernandez, Daniel David
1920 Lim, Chong Eang
1920 McHutcheson, George Browne
1920 van der Merwe, Frederick
1920 O’ Farrell, Patrick Theodore Joseph
1920 Renner, Edowo Awunor
1920 Vaughan, James Churchwill
1920 Waller, Harold William Leslie
1921 Allen, George Phillip Farmer
1921 Corfield, Charles Russell
1921 Hamid, Abdul
1921 Longhurst, Bell Wilmott
1921 Maevae, George Anthony
X921 Madan, Hans Raj
1921 Mulligan, William Percival
Date of
Diploma
1921 Nixon, Robert
1921 Richmond, Arthur Stanley
1921 Shri Kent, Shamsher Singh
1921 Skinner, James Maegregor
1921 Stewart, Robert Bell
1921 Thomson, Marion
1922 Bhatia, Jagat Ram
1922 Cohen, Morris Joshua
1922 Crawford, Andrew Clcmmcy
1922 Gilmore, Edward Raymond
1922 Gracias, Cajetan Manuel
1922 Jennings, Arthur Richard
1922 Lethem, William Ashley
1922 Paul, Sachchidananda Hoshen
1922 Pinder, John
1922 Rieley, Stanley Desmond
1922 Rutherford, Gladys
1922 Stewart, Quintin
1923 Abelman, B.
1923 Basu, Dhirendranath
1923 Cruickshank, John Cecil
1923 Doherty, Winifred Irene
1923 Edghill, Winifred M.
1923 Elsohn, John ,
1923 Fraser, N. D.
1923 Lee, R.
1923 Pierce, E. R.
1923 Raja, Rojaporum
1923 Reid, C. B. B.
1923 Richmond, A. E*
1923 Steven, J. B.
1923 White, Charles Francis
1924 Bilimoria, H. S.
1924 Carson, J. C.
1924 Chopra, B. L.
1924 Davis, B. L.
1924 Hardy, M. J.
1924 Jennings, C. B.
1924 Johnstone, F. J. C.
1924 Keirans, J. J.
1924 Lee, S. W. T.
1924 Macdonald, G.
1924 Maclean, G.
1924 Mathur, W. C.
1924 Mitchell, J. M.
1924 Owen, D. Uvedale
1924 Palmcr-Joncs, Beryl
1924 Sankeralli, E. J*
1924 Singh, H.
1924 Theron, Elizabeth M.
1925 Adams, Alfred Robert Davies
1925 Ashton, Frank Richard
1925 Ashworth, Esther
1925 Bamford, Charles Walker
1925 Beinashowitz, Jack
1925 Black, John
1925 Clark, George
1925 Coghlan, Bernard A.
1925 Collier, Ivy
1925 Crawford, £* J.
1925 Gumming, Patrick Grant
XU
Dait of
Pate of
Diploma
Diploma
1925
Ellano., Mary Muriel
1926
Rodrigues, N.
1925
Fither, Morris
1926
Sachdev, A. S.
* 9^5
Green, Frederick Norman
1926
Singh, B.
1915
Gnitu, M. S.
1926
Singh, J.
1925
Hawe, Albert J.
1926
Talib, S. A.
1925
Jafri, Z. H.
1926
Tan, C. L.
1925
Johnstone, Elvy I.
1926
Taylor, Catherine F.
1925
Kerr, James R-
1926
Turnbull, N. S.
1925
Mackay, Donald M.
1926
Turner, J. G. S.
1925
Mackay, E. K.
1926
Vardya, B. K.
1925
Makkawi, M.
Maldonado, Leopoldo Garcia
1926
Varma, T. N.
1925
1926
Voigt, C.
1925
* 9^5
Mar, Severn Francisco
Mozoomdar, B. P.
Shah, Khwaja Samad
1926
Wasti, S. N.
1925
1927
Allen, C. P.
1925
Skan, Douglas A.
1927
Bahl, M. L.
1925
Stone, Ernest R.
1927
Barrowman, B.
1925
Terrell, C. G.
1927
Bawa, H. S.
1925
Tooth, Frederick
1927
Bilimoria, J. D.
<925
de Waal, Jacobus Johannes
1927
1927
Burns, W. M.
Daly, E. J.
1926
Aitken, W. J.
1927
Dunlop, G. A.
1926
Ashworth, A.
1927
Dyream, V.
1926
Austin, T. A.
1927
Evans, R. R.
1926
Bansikar, R. N.
1927
Farid, M.
1926
Besson, W. W.
1927
Gillespie, A. M.
1926
Bligh-Peacock, R. N.
1927
Gimawardana, S. A.
1926
Bolton, EfBe G.
1927
Harkness, J.
1926
Boodrie, E. II.
1927
Hay, R.
1926
Brito-Mutunayagam, M. A. B.
1927
Ilodivala, N. M.
1926
Campbell, J. McP.
1927
Hughes, Emma
1926
Cullen, T.
1927
Hyslop, Kathleen IM.
1926
Davies, H. E.
1927
Ingram-Johnson, R. E.
1926
Dias, B. G. V.
Doherty, H. A. A.
1927
Kapadia, J. S.
1926
*927
Khan, F. A.
1926
Don, E. G.
1927
Khan, M. M.
1926
Earl, J. C. St. G.
1927
Labuschagne, P. N . H
1926
Fletcher, Beatrice N.
1927
Laird, W. J.
1926
Fowler, H. P.
1927
I^ewin, B. F.
1926
Fowler, Isabella J,
1927
Macdonald, J.
1926
Hamilton, J.
1927
McElroy, R. S.
1926
Hodgkinson, Katharine M.
1927
Maclay, W. S.
1926
Jackson, R.
1927
Maguire, H. O.
Mahaffy, A. F.
1926
Kamakaka, K. H.
1927
1926
Kennedy, J. H.
1927
Malhotra, A. II.
1926
Khatri, L. D.
1927
Malhotra, A. L.
1926
Lennox, D.
1927
Manghirmalani, B. S.
1926
Lewis, A. J.
1927
Meek, A. I.
1926
McConn, C. F.
1927
Mehra, J. N.
1926
Mackay, A/G.
1927
Mehta, H. C.
1926
McLean, N.
MacSwecncy, M.
1927
Menon, M. V.
1926
1927
Miller, H. V. R.
1926
Malhautra, K. L.
1927
Mokand, S. N.
Murgatroyd, F.
1926
MaUk, S. B.
1927
1926
Manuwa, S. L. A.
1927
Murray, A. J.
1926
Merchant, M. E.
1927
Murray, Pauline
1926
MitcheU, W. H.
Molony, E. F.
1927
Nevin, H. M.
1926
1927
Nirula, P. N.
1926
Nashikkar, S. G.
- 1927
Olusoga, N. T.
1926
Oppenheimer, F.
1927
Parakh, D. B.
1926
Ormiston, W. S.
1927
Peters, D. O.
1926
Paterson, F. S.
Patterson, F. L.
1927
Peters, M. R.
Pottinger, J. H.
1926
1927
1926
Pouri, V.
1927
Rao, R. S.
1926
Quigley, L. D.
1927
Rodriguez, G. V. S.
1926
Robertson, A.
1927
xiii
Shah, S. R. A.
Bate of
Diploma
192/ Singh, II.
1927 Southward, F.
1927 Sturton, S. D.
1927 Thompson, Frances C.
1927 de Villlers, B. J. van dc S.
1927 VValkinshaw, R.
1927 Wilkinson, S. A.
1928 Ahluwalia, C. L.
1928 Aidin, A. R.
1928 Anand, J. S.
1928 Askari, S. W. H.
1928 Beveridge, Ruby S.
1928 Biswas, M. K.
1928 Blakemore, W. L.
t928 Camps-Campins, J. M.
1928 Chacko, M. O.
1928 Chopra, A. N.
1928 Chaudhuri, J. P.
1928 Choudari, K. V. R.
1928 Cranage, Margaret
1928 Dhala, C. H.
1928 Dhar, K. K.
1928 Dikshit, II. K.
1928 Everard, N. J,
1928 Fine, J.
1928 Ghei, A. N,
1928 Halawani, A.
1928 Henshaw, L. E. R.
1928 Hilmy, I. S.
1928 Holmes, W. E.
1928 Hope-Gill, C. W.
1928 Kane, F.
1928 Katial, C. L.
1928 Khan, F. M.
1928 Krishna, R.
1928 I.awrcnce, H. S.
1928 Lawrence. M. R.
1928 McLaren, D. W.
1928 Malhotra, B. D.
1928 Mallick, B. I).
1928 Mason, Jean R.
1928 Menon, E. S. R.
1928 Milne, J.
Date of
Diploma
1928 Mitchell, A.
1928 Mone, R. V.
1928 Morley, A. H.
1928 Mostert, H. van R.
1928 Mufty, S.
1928 van Niekerk, S. V.
1928 Pandit, M. K.
1928 Pearce, W. T. A.
1928 Plum, D.
1928 Rao, B. D.
1928 Reid, A.
1928 Sanderson, I.
1928 Setna, II. M.
1928 Shearer, G.
1928 Singh, B.
1928 Sivalingam, S.
1928 Stratton, Ella M.
1928 Suri, R.
1928 Tuli, R. L.
1928 Udvadia, F. F.
1928 Wagle, P. M.
1928 Wahid, A.
1928 Wall-Mesham, Nellie
1928 Whig, P. L.
1929 Chakravarti, K. B.
1929 Crawford, J.
1929 Dale, W. C. '
1929 Dogra, J. R.
1929 I^rury, G. D.
1929 Gill, T. S.
1929 Herbertson, Margaret A. L
1929 Innes, J. A. I..
1929 McGregor, J. A.
1929 McQueen, W. B.
1929 Majumdar, B. K.
1929 Middleton, I. C.
1929 Pcarse, J. T. F.
1929 Ramdcholl, C.
1929 Robinson, Elizabeth J.
1929 Robinson, P. B.
1929 Shafi, A.
1929 Verghesc, T.
1929 Wilson, S. P.
The following have obtained the Diploma in Tropical Hygiene
of the University of Liverpool : —
. Diploma in Tropical Hygiene
Date of
Diploma
1926
Aitken, W. J.
Date of
Diploma
1926
MaeSweeney, M.
Oppenheimer, F.
1926
Bligh-Peacock, N.
1926
1926
Clark, G»
1926
Skan, D. A.
1926
Collier, Ivy
1926
Talib, S. A.
1926
Cullen, T.
1926
Turnbull, N. S.
1926
1926
Davis, B. L.
Don, £. G. A.
1927
Allen, C. P.
1926
Fowler, H. P.
1927
Austin, T. A.
1926
Hawe, A. J.
1927
Besson, W. W.
1926
Lennox, D.
1927
Dunlop, G. A.
1926
Mackay, A. G.
1927
Earl, J. C. St. G.
1926
Mackay, D. M.
1927
Hamilton, J.
1926
McLean, N.
1927
Harkness, J.
XIV
DaU iff
Difilmta
1927
Hay, R.
Date of
Diploma
1928
Maclay, W. S.
1927
Hyslop, Kathleen M.
1928
Miller, H. V. R.
1927
Labuschagne, P. N. H.
1928
Morley, A. H-
1927
McCon, C. F.
1928
Pcarson, G. H.
1927
Macdonald, J.
1928
Pottinger, J. H.
Mitchell, Winifred H.
1928
Sanderson, I.
^ 9*7
Murray, A. J.
1928
Sivalingam, S.
1927
Nevin, H. M.
1928
Wilkinson, S. A.
1927
1927
Nixon, R.
Ormiston, W. S.
1929
Askari, S. W. 11 .
1927
Robertson, A.
1929
Cole, H. A.
Drury, G. D.
1927
Walkingshaw, R.
1929
1928
Rilimoria, J. D.
1929
1929
Fraser, N. D.
Halawani, A.
192$
Blakemore, W. L.
Choudari, K. V. R.
1929
Hilniy, I. S-
1928
1929
Innes, J. A. L.
1928
Dhar, K. K.
1929
Lawrence, H. S-
Ramdeholl, C.
1928
Evans, R. R.
1929
1928
Holmes, W. E.
1929
Setna H- M.
1928
Laird, W. F.
XV
ANNALS OF TROPICAL MEDICINE .
AND PARASITOLOGY
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the paper, and arranged in the following way : —
Kobinson, S. (1914). The spleen in malaria. Ann, of Nosology,
20 , 20-25.
Smith, J. (1900). Enlargement of the spleen m malaria. Jl, of
Paihomeiry, 1 , 1-20.
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xvi
SUSCEPTIBILITY AND RESISTANCE TO
TRYPANOSOME INFECTION
VI.— THE COURSE OF THE INFECTION IN
SPLENECTOMIZED RATS
BY
1 . J. KLIGLER
{Department of Hygiene, Hebrew University, Jerusalem)
{Received for publication 2 May, 1929)
In the preceding paper (1929) it was pointed out that the rat
offered a type of resistance similar in kind, but different in degree
from that observed in the guinea-pig. It was also indicated that this
resistance was probably referable to the reticulo-endothelial system.
It seemed of interest, therefore, to observe the course of infection
in splenectomized rats. It was apparent that if the contention was
correct, splenectomized rats should react in the same manner as the
mouse, that is, the rate of multiplication of the trypanosomes should
be uniform and follow a line of geometric progression.
There was a serious difficulty in carrying out this experiment.
The splenectomized rats developed an acute Bartonella infection
and succumbed in five or six days, before the trypanosome infection
had run its course.
This difficulty was eliminated by the observation made by Meyer
(1927) that an injection of salvarsan prior to the removal of the
spleen prevented the appearance of Bartonella for some time. Using
this procedure it was possible to observe the course of infection in
splenectomized rats without interference of other factors.
The results of tJiese experiments constitute tAe suSfecif 0/
this paper.
315
3i6
EXPERIMENTAL
Series i. Large rats, 120 to 150 grams in weight, were
used. These were divided into three groups. One set received
0*5 c.c. of a I : 1,000 solution of Neosalvarsan intraperitoneally and
the spleen was removed two or three days later. A second set
was splenectomized without previous treatment with salvarsan.
The third set served as a control.
Two sets of experiments were carried out, identical in all essentials,
except that in one a small dose of trypanosomes was injected sub-
cutaneously, while in the other a somewhat larger dose was inoculated
intraperitoneally. In a number of rats in each experiment, red cell
and trypanosome counts were made daily. In the others only the
incubation period and the end results were noted. T. evansi was
used in all experiments.
The results were striking and consistent. The untreated
splenectomized rats developed a Bartonella infection and in most
cases died with a severe anaemia either before the trypanosome
infection had developed or during its progress. In the splenecto-
mized animals treated with neosalvarsan neither the Bartonella
infection nor anaemia developed. On the contrary, the anaemia,
which is usually associated with a trypanosome infection, was not
observed in the salvarsan treated animals.
In all of the animals the course of the infection differed decidedly
with the method of inoculation. The control animals differed,
however, in this respect from the splenectomized ones. In the
former the course of infection was more rapid when the infection
wa^ by the subcutaneous route, while in the latter the reverse was
the case.
The results of these experiments are presented below (p. 317).
It will be noted that there was practically no difference in the
incubation period and duration of illness between the salvarsan-
treated splenectomized rats and the control. Nor was there any
difference in the course of the infection. The only striking difference
is that in the salvarsan-treated animals the red cell count at death
was nearly 8,000,000 (the normal count), while in the control group
it was reduced to 5,000,000.
Quite a different result was obtained when the infection was
given by the intraperitoneal route.
3*7
Tabli Ia.
Effect of splenectomy on a trypanosome infection in rats. (Infected subcutaneously.)
Number
of
rats
Average
weight
Mode
of infec-
tion
Dose
Splc'
necto-
mized
Sal-
varsan
Average
incuba-
tion
Average
duration
of
illness
Average
tryp.
count
at death
Average
red cell
count
at death
5
142
Subcut.
10,000
+ i
+
6.4
* 3-4
1,860,000
7,975,000
5
136
))
10,000
+
*6.0
* 900,000
2,300,000
5
137
}j
10,000
Con trol
1
6.0
14.0
1,700,000 i
5,100,000
• Only one animal survived, all the others died five to six days after the spleen was removed, with a
red cell Co\int of 1,800,000; the remaining animal died before the trypanosome infection had run
its course.
Table Ib.
Effect of splenectomy on a trypanosome infection in rats. (Infected intraperitoneally.)
Number
of
rats
Average
weight
Mode
of Infec-
tion
1 ;
1 Splc Sal-
Dose 1 necto- varsan
j mized ,
Average
incuba-
tion
Average
duration
of
illness
Average
tryp.
count
at death
Average
red cell
count
at death
4
141
Intra-
f I
65,000 +14-!
3cl.
7 i
1,900,000
6,200,000
pcr.
i j
5 *
136
65,000 ' + —
3
* 500,000
1,650,000
4
124
-
»»
1
65,000 Con Irol
j
5
*5
1,800,000
4,600,000
•Two died before the onset and three in the middle of the infection.
In this series "the course of the infection in the splenectomized
rats was strikingly different from that in the control. The incubation
period as well as the duration of the infection was only half as long
as in the control group. Again, the red cell count at death in the
salvarsan-treated animals was relatively high as compared with that
of the control untreated animals. Typical detail data of the course
of infection in the two series are shown in Tables II and IIa.
3i8
Table II.
Course of infection in splencctomized and control rats infected intraperitoneally
with same dose of T. evansl.
(Infected 17 January.)
Splencctomized -f- salvarsan
Control (no salvarsan)
142 grm.
145 grm.
126 grm.
122 grm.
Jan. 20
+ in drop
-f- in drop
-j- in drop
-j- in drop
Jan. 21
4,000
2,000
— in drop
— in drop
Jan. 22
42,000
44,000
2,000
— in drop
Jan. 23
438,000
478,000
2,000
-f in drop
Jan. 24
a.m.
1,200,000
1,900,000
-f- in. drop
p.m.
1,600,000
2,200,000
...
...
Jan. 25 '
died 24-25
died 24-25
16,000
2,000
Jan. 27
82,000
2,000
Jan. 28 i
100,000
10,000
Jan. 29
700,000
...
Jan. 30
...
1,800,000
250,000
J?”- 3'
• ••
died 30-31
700,000
Icb. I
...
900,000
died 1-2
Table 11a.
Same as above, Infection subcutaneous with same dose of T. evansi.
(Infected 14 January.)
Date
Splencctomized -f- salvarsan
Control (no salvarsan)
145 grm.
145 grm.
136 grm.
145 Srm,
’Jan. 20
—
• • •
-f in drop
Jan. 21
—
—
+ in drop
—
Jan. 22
2,000
8,000
in drop
...
Jan. 23
12,000
6,000
10,000
32,000
Jan. 24
4,000
--
4,000
20,000
Jan. 25 ;
6,000
20,000
-1-4,000
12,000
Jan. 26
Jan. 27
Jan. 28
400,000
220,000
160,000
330,000
a.m.
950,000
1,300,000
130,000
3 50,000
p.m.
1,600,000
died 28-29
1,400,000
died 6 p.m.
....
...
Jan. *9
Jan. 30
...
300,000
1,600,000
a.m.
•
1,650,000
1,670,000
died 10 a.m.
p.m.
...
...
1,800,000
died 30-31
...
319
Summarising these experiments it appears that (i) Splenectomized
animals treated with salvarsan and infected by the subcutaneous
route did not show any decreased resistance as compared with the
corresponding untreated control group ; (2) However, animals so
treated and infected by the intraperitoneal route manifested a
striking reduction in resistance as compared with the corresponding
control group, the course of the infection being the same as that
observed by Doerr and Berger (1922) in mice ; (3) The salvarsan not
only prevented the development of Bartonella infection for over two
weeks, but it seemed also to protect the red cells against the
destructive effects of the trypanosome infection ; (4) Death in
tr5^anosome infections was apparently not affected by the absence
of anaemia.
Series 2. These experiments were repeated with the same results.
The following experiment is illustrative. The procedure was the
same as above, except that the same doses were given intra-
peritoneally and subcutaneously, and all the animals were inoculated
at the same time with the same material. The data of this experi-
ment are summarised in Tables III and IV.
Table III.
Comparison of the duration of infection in splenectomized, salvarsan-treatcd and normal rats.
Treatment
Mode of
inocula-
tion
Dose
Average
weight
Average
incuba-
tion.
Dap :
Average
duration
of illness.
Days
Final
tryp.
count ;
average
Initial
red cell
count ;
average
Final
red cell
count ;
average
0.3 C.C., 1 : 1,000 sol. neo-
salvarsan i.p., 5.ii.28 ;
Splenectomy, d.ii.zS ;
Infection, 7.ii.28
Subcu-
taneous
25,000
26.5
4
1,850,000
4,300,000
3,900,000
Salvarsan as above, 5.ii.28 ;
Spleen not removed. In-
fected, 7.ii.28.
25,000
26.5
6
i8i
1,800,000
4,500,000
4,700,000
Untreated Control ; Iri-
fected, 7.ii.28.
25,000
24.0
5
10^
1,850,000
4,250,000
3,250,000
0.3 C.C., I : 1,000 sol. neo-
salvarsan i.p., 5.ii.28 ;
Splenectomy, b.ii.aS ;
Infection, 7.ii.28.
Intra-
perit.
25,000
26.0
3
8
1,450,000
4,550,000
3,100,000
Salvarsan as above, 5.11.28 ;
Spleen not removed ;
Infected, 7.ii.28.
j)
25,000
27-5
S
m i
1,800,000
5,000,000
3,750,000
Untreated Control \ In-
fected, 7.11.28.
25,000
22.0
4
13 ^
2,200,000
4,800,000
3,200,000
0.3 C.C., I ; 1,000 sol. neo-
salvamn} Spleen re- |
moved, 6.U.28 ; Not in-
fected.
4,700,000
6,100,000
(2i.ii.28)
320
Table IV.
Median course of infection in splenectomized, salvarsan treated and normal rats.
(Infected February 7, a.m..)
Daily trypanosome count — per c. mm.
Date
Splenectomized rati
treated with salvarsan
Control rats
Salvarsan treated
normal rats
Intra-
Sub-
Intra-
Sub- 1
Intra-
Sub-
peritoneally
cutaneously
peritoneally
cutaneously
. j
peritoneally
cutaneously
Feb. 10
-)- in drop
...
...
-j- in drop
...
Feb. 12
! 8,000
4" in drop
-f- in drop
in drop
4,000
...
Feb. 13
92,000
-f- in drop
-{- in drop
-
~
-f- in drop
Feb. 14
466,000
-f* in drop
6,000
34,000
2,000
2,000
Feb. IS
1,000,000
died I p.m.
2,000
4,000
80,000
2,000
8,000
Feb. 16
...
...
460,000
...
26,000
Feb. 17
80,000
Sjooo
700,000
^,000
16,000
Feb. 18
...
160,066
16,000
2,500,000
8,000
30,000
Feb. 19
...
750,000
44,000
18,000
24,000
Feb. 20
...
1,200,000
died 10 p.m.
300,000
...
22,000
42,000
Feb. 21
650,000
1 1 2,000
1 50,000
Feb. 22
1
...
1,800,000
died 2 p.m.
1,000,000
died 12 p.m.
350,000
died 25.1!,
2 p.m.
Note. — The counts were all made at the same time — between 8 and 9 a.m.
It is clear from these tables that splenectomized rats infected
by the intraperitoneal route succumbed long before those infected
subcutaneously or the corresponding controls. In normal rats the
mode of inoculation also materially affected the course of the infect
tion, but in an opposite manner : those infected by the subcutaneous
route succumbed sooner than those receiving the same dose intra-
peritoneally. Another important point brought out in these
experiments is that the salvarsan injection, as such, modified the
course of infection in normal animals, but that this effect was either
not apparent (intraperitoneal infection) or greatly reduced (sub-
cutaneous infection) in the splenectomized rats.
Chart I. Course of Infection in rats treated as indicated and inoculated intraperitoneally. (The
animals were of the same weight and received the same dose of T. evansi jXi.zB.)
322
Chart IT. Course of infection in rats treated as indicated and inoculated subcutaneously. (The
animals were of the same weight and received the same dose of T. evansi 7.ii,28)
3^3
The detailed course of the infection in splenectomized and non-
splenectomized animals infected by various routes is shown in
Table IV and Charts I and TI. It is apparent that in splenectomized
animals inoculated intraperitoneally the native resistance is almost
completely broken down despite the salvarsan. Both the generation
time and the curve of multiplication of the trypanosomes in the
peripheral circulation correspond with that usually observed in mice.
DISCUSSION
The experiments reported above bring to light a number of
significant facts. It appears that in normal rats the resistance to a
trypanosome infection is highly localised, the chief organ of defence
being the spleen. Normal animals infected subcutaneously succumb
much sooner than those inoculated intraperitoneally. In salvarsan-
treated animals the opposite is the case. But, when salvarsan-
treated rats are splenectomized, then the results are again reversed.
Despite the salvarsan, the animals infected intraperitoneally lose all
resistance to infection ; at the same time, the resistance to a sub-
cutaneous infection seems to be greater than that of untreated
controls.
This peculiar behaviour of salvarsan is particularly interesting
in relation to the mechanism of chemotherapy. Krichewski and
Meersohn {1926) first showed that the reticulo-endothelial system,
particularly the spleen, plays a definite part in the therapeutic effect
of salvarsan. Subsequently, Feldt and Schott (1927), Jungblut
(1927), as well as Kritchewski (1927) showed that this is also true of
other drugs. Kritchewski (1927, 1928) expressed the view that the
spleen acts merely as a carrier of the drug, storing it up and then
slowly liberating it. The heightened resistance to the subcutaneous
hifection in comparison with normal controls and the suppression
of the Bartonella would indicate that even in splenectomized animals
the salvarsan is stored and is active despite the removal of the
spleen. Its activity is entirely absent only in splenectomized
animals infected intraperitoneally. But this merely emphasizes
the importance of the spleen as an active participant in the thera-
peutic action of the drug. Evidently other parts of the reticulo-
endothelial system also play a part.
3H
Another interesting point is the apparently protective effect
of salvarsan on the red cells. Anaemia is a characteristic element
in the pathology of a trypanosome infection. In the above experi-
ments the salvarsan-treated animals did not show the typical picture.
On the contrary, there appeared to be a stimulation of the red cells.
It would seem possible that the prevention of the Bartonella may
be due to this protective action of the drug on the red cells. This
possibility is supported by the fact that as soon as the salvarsan
effect disappears — usually about three weeks — the Bartonella appear
and the animals succumb in five or six days.
CONCLUSIONS
1. Salvarsan increases the resistance of normal rats to a trypano-
some infection and appears to exert a protective effect on the red
blood cells. The former effect is either absent or greatly reduced
in splenectomized rats.
2. Splenectomized rats treated with neosalvarsan to prevent
a Bartonella infection, show a complete absence of resistance to a
trypanosome infection when the inoculation is given intraperitoneally.
The course of infection in such rats follows a simple curve of geometric
progression.
3. No corresponding reduction in resistance is noted in such
rats when the inoculation is given subcutaneously. This is
apparently attributable to the action of the salvarsan.
4. In normal rats the course of the infection is more rapid if the
inoculum is given subcutaneously than it is when given intra-
periteonally.
REFERENCES
Doerr, R., and Berger, W. (igaz). Bezichungen zwischen Virulcnz und Vermehrungsgeschwindigkeit
der Erreger. Dargestellt an der Naganainfektion dcr weissen Maus. Ztschr/f. Hyg.^ 95, 319
Felot, a., and Schott, A. (1927). Die Rolle des Retikuloendothcls beim chemotherapeutischen
Hcilungsvorgange. Ztscbr. /. //jyg., 107, 453.
JuNGiBLUT, C. W. (1927). Ueber die Bezichungen zwischen retikuloendothelialem System und
chcmotherapeutischer Wirkung. Ztscbr. f, Hyg.y 107, 357.
Kligler, I. Jr, and Comaroff, R. (1929). Susceptibility and resistance to Trypanosome infections.
V. — The resistance of rats to infection. Aft». Trap. Med. Parasitol.^ 23, 103.
Kritschewski, I. L. (1927)- Das retikulo-endothelialc System und Cheraotherapic. Qentralbl.f.
Bfikt. Orig., 104, 214. t .
(1928). Ueber noch unbekannte Funktion des retikuloendothelialen Systems. V. — Der
Mechaniamus der die Aktivitat des chemotherapeutischen Effektes bestimmenden- Funktion
des retikulo-endothelialen Systems und ihrc Unabhangigkeit von der Scliutzfunktion.
Ztscbr. f. Immunity tsf.f 59, i.
and Meersohn, I. S. (1926). Ueber die Zusammenh singe zwischen dem therapeutischen
Effekt und dem retikuloendothelialen Appamt. Ztscbr. f. Jmmunitdtsf., 47, 407,
SUSCEPTIBILITY AND RESISTANCE TO
TRYPANOSOME INFECTIONS*
VII.— CAUSE OF INJURY AND DEATH IN
TRYPANOSOME INFECTED RATS
BY
I. J. KLIGLER,
A. GEIGER
AND
R. COMAROFF
{Department of Hygiene, Hebrew University, Jerusalem)
{Received for publication 6 May, 1929)
The cause of death in experimental trypanosome infections
has been a subject of considerable discussion. The infection in
the rat is relatively so simple that many investigators have turned
their attention to a study of the course of a trypanosome infection
in this animal in the hope of elucidating the mechanism of injury
and death in trypanosome and allied infections.
Two opposing views have evolved. Schilling and Rondoni
(1913), Martin and Darre (1914), Reichenow (1921), and more
recently, Regendanz and Tropp (1927) assume that the injury and
ultimate death are due to a toxic substance liberated by the dis-
integration of the parasites. Reichenow finds support for this view
in the fact that in man the height of the temperature is reached after
the trypanosomes disappear from the circulation.
On the other hand, Schem (1926, 1928) and Fenyvessy (1926)
maintain that the cause of injury and ultimate death is to be found
in the exhaustion of the blood sugar and glycogen reserve. These
authors found that not only do trypanosomes utilize sugar in vitro,
- ’ • A pfeliminary report of a part of thU work was published by Kllglcr, I. J., and Geiger, A. (1928),
in the Prdr. of the Sbc. Exp, Biol, and Medicine, 26 ) 229. *
325
326
but that a definite hypoglykemia develops in the infected animal
in the course of the infection. Regendanz and Tropp (1927), who
support the toxin theory, were able to confirm the findings of Schern
and Fenyvessy, but their results indicate that the glycogen depletion
is by no means complete and that at the height of the infection
sufficient glycogen remains in the liver to maintain a normal sugar
concentration in the blood. They maintain that the decrease in the
blood sugar is due to a depressive effect on sugar inversion by the
trypanosome toxin and not to the depletion of glycogen.
In further extension of his views, Fenyvessy (1927) studied
the respiratory exchange of infected animals and published data
which indicate a more active metabolism in trypanosome infected
animals than in normal ones, particularly towards the end of the
infection. His data show that the oxygen consumption of infected
animals increases with the increase in the number of trypanosomes
in the blood, and he concluded that this increase is due directly to the
metabolism of the trypanosomes. Scheff (1928), in continuation
of Fenyvessy’s work, found further that there is a greater utilization
of the blood oxygen in trypanosome infected than in normal rats,
and a progressive decrease in the oxygen saturation of the blood.
It is clear, therefore, that there exist two opposing views. One
ascribes the changes to the action of a toxin, the other to the direct
injury due to the sugar depletion by the metabolic activity of the
trypanosomes. Neither view is adequately supported by experi-
mental facts. There is also a discrepancy in the analytical data
reported by Regendanz and Tropp (1927) and those by Schern (1928)
and Scheff (1928). The data presented by the former show that
there is only a partial glycogen exhaustion, while the latter claim
that the exhaustion is complete. At the same time, Scheff (1928)
states that he is unable to account for the fact that the cure of a
heavily infected animal with * Bayer ' or other drug leads to a prompt
recovery of the blood sugar concentration to normal.
One aspect of the problem seems to have escaped the previous
workers. Although there is general agreement that the blood sugar
concentration is depressed, no attention has been given to the
possible harmful effect of intermediate prod\icts of the sugar meta-
bolism. It seemed to us more than likely that the depression of
jthe sugar conpentration in the blood was due to its active utilization
3^7
by the trypanosomes, so active that readjustment could not keep
pace ; and that this active glucose metabolism led to a state of
constant high lactic acid concentration in the blood. This view
would account also for the prompt equalization of the blood sugar
after the tr3^anosomes had been eliminated by a drug or otherwise.
We, therefore, decided to determine the lactic acid concentration
and alkali reserve in the blood at various stages of the infection.
In this paper we deal specifically with the lactic acid concentration.
EXPERIMENTAL
Preliminary to the main object of this investigation, we attempted
to test the opposing views in a direct manner. We also attempted
to repeat Fenyvessy's metabolism experiments.
Toxic Effect of Trypanosomes, Massive doses of trypanosomes
were injected repeatedly into rats. No ill-effects were noted.
The same results were obtained by injection of serum obtained from
infected rats shortly before death. The following protocols are
typical of several experiments with the same results.
A heavily-infected guinea-pig was bled into citrate solution.
The blood was sedimented at low speed, to throw down the red cells.
The supernatent fluid was sedimented at high speed and the sedi-
mented trypanosomes separated from the clear fluid. The sediment
was re-suspended in a small amount of distilled water and stored
in the ice-box. The supernatent serum was also stored.
The trypanosomes and plasma respectively were injected
repeatedly into a series of rabbits and rats. Control animals were
given saline injection. The experiments were repeated with
r. evansi, T. gambiense, and T. rhodesiense.
The T. gamhiense treated animals were given seven injections,
the others received ten injections, in the course of two weeks. In
the rabbits the injection of the autolized trypanosomes and, to some
extent, also the plasma, was associated with a leucopenia. No
other toxic manifestation was observed either in the rats or rabbits.
On subsequent infection of the rats with the homologous strain,
the treated animals died at the same time or a day or two before
the controls.
328
It seems, therefore, that even the repeated injection of heavy
doses of trypanosomes does not exert an appreciable toxic effect
on the animal. At any rate, the toxic effect is not sufficient to
account for the severe damage and ultimate death caused by the
infection.
The Effect of Supplementary Injections of Glucose. If carbo-
hydrate depletion is the direct cause of injury and death, then
daily injections of glucose should at least modify the course of the
illness. A series of experiments were made to test this assumption.
The results are shown in the following table.
Iable I.
Effect of glucose injections into rats on the course of a Trypanosome infection.
Number
of
rats
Weight
in grms.,
average
Dose
Date
infected
Incuba-
tion
time,
days
Duration
of
infection,
days
'Freatment
2
53-5
1 50,000
3.vi.28
5
* 7-5
Untreated
2
53-5
1 50,000
3.vi.28
5
19.5
0.5 c.c. 10% glucose* sol.
from 3I.V.28 to end
5
33-2
10,000
22.vi.28
11
15.0
Untreated
33-3
10,000
22.vi.28
10
15-0
0.5 c.c. 10% glucose sol.
daily from 4.vii.28 to end
6
33.2
, 50,000
28.xl.28
3.5
8.5
Untreated
,6
33-2
50,000
28.xi.28
3.0
8.7
1
0.5 c.c. 10% sol. of glucose
daily from i.xit.28 to end
5 1
33-4
50,000
13.xi.28
S.8
16.0
Untreated
5
1
33-6
i
50,000 ;
13.xi.28
6.0
13.0
0.5 c.c. 10% glucose
daily from 19.xi.28 to end
6
36-3
16,000
25.i.29
4.0
00
Untreated
6
4 *-S
16,000
j
25.1.29
4.5
22.8
0.5 c.c. glucose injection
tv^dee daily^ and 1*0
glucose supplementary
to diet ; Dinning 2
days after the infection
~ to the end
32 $
The results indicated an advantage when the glucose treatment
was begun before or at the beginning of the infection. The groups
which were given glucose from the time that trypanosomes first
appeared in the circulation, that is at the end of the incubation
period, showed no advantage over the untreated group. In the
three series in which the glucose injections were begun at the onset
of the infection, the average duration of the infection in the untreated
rats was 12*9 days, while in the -treated ones it was 12*2 days. In
the two other series the advantage is definitely with those rats
which received glucose — 17-7 days against 22 days.
Respiratory Exchange of Trypanosome Infected Animals. The
respiratory exchange was studied on a large series of infected rats.
To eliminate errors in experimentation the normal animals were
first accustomed to the apparatus. At the beginning the animals
were extremely restless. After several tests, however, they remained
perfectly quiet even for several hours. Observations were first made
on normal animals which had become accustomed to the apparatus ;
these animals were then infected and the respiratory exchange
measured at various stages of the infection as determined by direct
chamber counts. The infecting dose was small (25,000 Tr.) in
order to prolong*the duration of the illness.
The apparatus used for the respiration experiments is a modifica-
tion of the Benedict apparatus devised by Geiger. In several
instances the Haldane apparatus was used as a control. The results
obtained with the two systems were in entire agreement. The
animals remained in the apparatus at least two hours, and each
time the apparatus was tested before and after the experiment to
assure absence of leakage.
One would assume, on the basis of the observations made by
Nauss and Yorke (1911) and others, that trypanosomes consumed
oxygen in vitro, that in vivo as well their activity would be marked
by a higher oxygen consumption by the animal. This, however,
we failed to observe in many oft-repeated tests. There appears,
on the contrary, a depression in activity, the reason for which is
not clear ; this question will be discussed more fully below.
The results are shown in Table II. It is apparent that there is
no increase in oxygen consumption in trypanosome infected rats,
as compared with normal ones. On the contrary, there seems
330
often, in the last stages of the infection, to be a lowered oxygen
consumption. It should be noted that we used a species of trypano-
some different from that of Fenyvessy. In all our experiments we
used the strain of T. evansi which had been isolated by us (Kligler and
Weitzmann, 1924) about five years ago, from mules.
Table II.
Respiratory exchange in trypanosome infected rats.
Number
of
rat
Day of
examination
Weight
in
grammes
Oa consumed
per hour
per kilo.
Respiratory
quotient
[
Number of '
trypanosomes !
per cubic mm.
of blood
Date
of
death
McCollum
|Diet —
Old
rats
!
3*»v.28
185
1,377 C.C.
0.81
0
X
9.iv.28
184
*.383 »
0.80
0
I
27.iv.28
181
1,381 „
i 0.78
i 48,000
i.v.28
*
30.iv.28
181
*1367 »
0-79
1 , 1 66,000
2
3.iv.28
179
1,379 c-c-
0.86
0
2
1 5.iv,28
178
h^77 »
0.83
0
2
27.iv.28
176
1 *,369 »
0.80
8,000
3.V.28
2
30.iv.28
176
*.350 »
0-77
60,000
Young
rats.
3
^.li.28
96
2,080 c.c.
0.86
0
3
().ii.28
96
2,080 ,,
0.86
0
h.lii.zS
3
14.ii.28
102
2.128 „
0.88
0
3
28.ii.28
102
2,082 „
0.80
Infected
3
3.iii.28
102
1 *j 904 »
0.82
Heavy infection
4
7.ii.28
II2
1,972 c.c.
0.88 i
0
4
27.ii.28
I I I
1,962 „
0.89
Heavy infection
28.il.28
4
28.ii.28
III
1,622 „ j
0.71
Heavy infection
2 hours before
1 death
5
29.1.28
130
1,873 C.C.
0.83
0
5
3.ii.28
13*
*j 943 »
0.80
0
4.111.28
• 5
2.iii.28
*32
1,940 „
0.77
Heavy infection
Salt Poor
Diet —
Sodium
poor diet
6
29.iii.28
181
1,490 c.c. 1
0.71
0
6
29.iv.28
*83 1
00
0*74
700,000 ^
I.V.28
6
30.iv.28
182 j
*,479 »
0.72
1,600,000
7
22.iv.28
136
1,531 c.c.
0.87
0
30.iv.28
7
29.iv.28
132
*,49* »
0.79
1,034,000
Potassium
poor diet
8
30.iii.28
148
1,800 c.c.
0.81
0
8
i.iv.28
148
1,872 ,,
0.88
0
29.iv.28
8
29.iv.28
*32
1,890 „
0.81
1,034,000
9
30.iii.28
132
1 1,580 c.c.
0.81
0
9
i.iv.28
*32
*,642 „
0.84
0
9
29.iv.28
*32
1,621 „
0.79
734,000
331
Lactic Acid Production. The negative results obtained in the
experiments reported above and more particularly the absence
of an increase in the respiratory exchange of infected animals,
strengthened our first assumption, that incompletely oxidised
metabolic products of glucose, probably lactic acid, resulted from the
activity of the trypanosomes and gave rise to an acidosis. We,
therefore, directed our attention to the presence of lactic acid in
infected animals.
The quantitative determination of lactic acid in the blood is a
somewhat complicated procedure, and care must be taken to prevent
any convulsive movements on the part of the animals which, in them-
selves, would cause a rapid rise in the lactic acid content. The
procedure adopted was as follows : — The animal was starved twelve
hours before being bled. It was then placed under a beaker con-
taining a cotton wad soaked in ether. The animal dozed off slowly
with relatively few movements, and in about one minute was in deep
narcosis. It was immediately placed on the board, a thin canula
inserted in the carotid artery and the blood withdrawn with a glass
syringe. After a little practice the whole procedure lasted only a
few minutes.
The arterial blood was examined by the method described by
Friedmann, Cotonio and Shaffer (1927). Heparin was used to prevent
coagulation.
Before the tests were made on infected animals, a series of
normal animals were examined by the same procedure. Likewise,
each time a normal control was run to check the procedure. The
results seem, therefore, relatively free of error.
At the time when blood was taken for lactic acid determination,
a red cell count, haemoglobin determination and trypanosome
count were made. The lactic acid data could, therefore, be correlated
with other findings.
The results are shown in Table III. In the first part of the table
are cited data for normal animals. The average red cell count is
about 7,000,000, the haemoglobin index over 90, and the lactic
content 30 mgm. per 100 c.c. of blood. In the infected animals
there is a progressive decrease in the red cell count with the increase
in the number of trypanosomes, the haemoglobin index is only
$lightly reduced^ but there is a definite progressive rise in the lactic
332
acid concentration parallel to the rise in the number of trypanosomes.
In instances where the animal is approaching exitus — Nos. 15
and 16 — the amount of lactic acid is relatively enormous, three to four
times the normal concentration.
Table III.
Lactic acid in normal and trypanosome infected blood.
Rate
Number of
trypanosomes
per c.mm.
Number of
red cells
per c.mm.
Haemoglobin
index ;
Sahli
Lactic acid ;
mgm. in
100 c.c. blood
1.
Normal
7,000,000
95
35-0
2.
7,500,000
98
29.0
3 -
29-5
4.
6,800,000
92
27.7
5 -
6,450,000
86
26.0
Average
...
30
I.
'I'ryp. Inf.
10,000
8,000,000
29.6
2.
J3 3>
12,000
6,500,000
52.7
3 -
J) 35
50,000
7,700,000 1
I
57-0
4 -
33 33
56,000
1
6,600,000
00
58.0
5 -
33 33
118,000
7,000,000
7 «
72.6
6 .
53 33
120,000
7,000,000
86
72.0
7 -
33 55
300,000
6,000,000
78
43-0
8.
33 33
300,000
...
30.8
9 -
33 3,
668,000
5,800,000
80
4S.2
10.
33 33
1
1,080,000
78
103.0
II.
33 33
1,180,000
...
8^
106.0
12.
33 33
1,450,000
5,000,000
80
94.0
» 3 -
33 33
1,600,000
7,000,000
...
87.0
14.
33 33
1,650,000
5,000,000
...
lOI.O
* 5 -
33 33
1,850,000
4,000,66b
62
120
333
It would seem, therefore, that the trypanosome infected animal
is constantly in a state of acidosis even when the number of organisms
is still relatively small, 50,000 to 100,000 per c.mm. Whether
the lactic acid is due directly to the trypanosomes or indirectly to an
impairment in the oxidative processes of the tissues, is not clear.
In either case, there seems to be an insufficiency in the oxidative
mechanism to complete the oxidation of the lactic acid. This is
in harmony with the data on the respiratory quotient recorded above.
Nor is the reason for the lowered oxidation quite clear. The
decrease in the number of red cells does not account fully for this
phenomenon because the red cells are decreased rather slowly at
first and only towards the end is there a sharp and sudden diminution
in their numbers. Two possibilities present themselves. One is
that there is a rapid consumption of oxygen by the trypanosomes,
leading to a lowering in the oxygen tension of the blood and depriving
the tissues of their needed oxygen. In favour of this view is the
drop in the oxygen saturation of the blood in infected animals
observed by Scheff (1928). The data reported by this author show,
however, considerable variations and our own observations thus far
reveal very little difference in the oxygen content of the arterial blood
of normal and infected rats.
The other possibility is that the lactic acid is produced continually
by the trypanosomes and too rapidly for complete oxidation and
that the lactic acid in turn affects the oxidative process. Thus a
vicious circle is established. This view is partly supported by the
observations made by Geiger (1929) that in vitro certain anions, and
particularly lactate, deflect the isoelectric point of haemoglobin.
This effect is, however, dependent on the concentration of the
anion, and it is doubtful whether in the early stages of the infection
this constitutes the most important phase. The process is obviously
a cumulative one beginning with a rapid and continuous production
of lactic acid, leading probably to a progressive depletion of the
alkali reserve, a reduced oxidation and a still greater accumulation
of lactic acid, resulting in further depletion of the alkali reserve and
depression of the normal oxidative processes ; death finally resulting
from asphyxia.
That the acidosis plays a considerable part in the pathology of the
disease is indicated by experiments now under way. Two sets
334
of five rats of the same weight were infected at the same time with
T, evansi ; one set was untreated and the other received twice daily,
0*5 c.c. 10 per cent, bicarbonate solution intraperitoneally. In spite
of the evident injury due to excessive bicarbonate, the average
duration of life in the control group was i8 days, and in the bicar-
bonate treated group, 26*5 days — almost a 50 per cent, increase in the
duration of life. These results are very suggestive.
CONCLUSIONS
1. Injection of large doses of trypanosomes, or serum taken
when the trypanosome number is at its maximum, does not produce
any visible toxic symptoms in rats.
2. Daily injection of glucose to supplement the food affects
the course of infection favourably only if started' at the time of
inoculation and not if started after the incubation period.
3. The oxygen consumption of trypanosome infected rats is not
increased ; towards the end of the infection it appears somewhat
lower than normal.
4. Parallel with the increase in the number of trypanosomes,
there is a progressive increase in the concentration of lactic acid in the
blood — in the later stages up to three or four times the normal.
5. It is suggested that the pathological processes are engendered
by the metabolism of the trypanosomes which results in the rapid
production of lactic acid, leading to exhaustion of the alkali reserve
and probably also to a depression of the oxidative processes by the
specific effect of lactic acid on the haemoglobin.
6. Experiments are under way which indicate that injection of
bicarbonate tends to increase the life of the animals as compared
with the untreated controls.
REFERENCES
Fenyvessy, B. von (1926). Ueber die Bedeutung des Stoifwechsels der Paraaiten fiir das Wirtsticr
bei der Trypanosomeiiinfektion. Biochem. Ztsebr.^ 1T3» 289.
• and Reiner, L. (1927). Untersuchungen iibw dca respiratozischen Stoilwechacl der
Trypanosomen. Ztsckr. f. Hyg,j 102, 109.
Friedman, T. E., Cotonio, M., and SuAFriR, P. A. {1927). llie determination of lactic acid.
Biol. Cbem.^ 73, 335.
335
Geioer, a. (1929). In press.
Ki.lGi.ER, T. J., and Weitzman, I. {1924). Susceptibility and resistance to Trypanosome infections.
I. — Attempts at immunization with dead and attenuated Trypanosomes. Jnn. Trop. Med, &
Parasttol.y 20 , 147.
Martin, L., and Darr^, H. (1914). Documents sur la trypanosomiasc humalne. Bull. Soc. Path,
Exot., 7 , 71 1.
Nauss, R. W., and Yorke, Warrington (1911). Reducing action of Trypanosomes on Haemoglobin.
Sleep, Sick. Bull. (31), 5 , 411.
Regendanz, P., and Tropp, C. Das Verhalten des Blutzuckers und des Leberglykogens bci mlt
Trypanosomen infizierten Ratten. Arch. f. Schiff's-u. Trop.-Hyg.y 31 , 376
Reichenow, E. (1921). Untersuchungen iiber das Verhalten von Trypanosoma gambiense in
menschlichen Korper. Ztschr.f. Hyg.f 94 , 266
ScHEFF, G. (1928). Ueber den intermediaren Stoffwcchsel der mit Trypanosomen infizierten
Ratten. Biochem. Ztschr.j 200 , 309.
ScHERN, K. (1911). Ueber die Wirkung von Serum und Leberextrakten auf Trypanosomen. Arb,
a. d. Kaiserl. Gesund., 38 , 338.
• (1925)- Ueber Trypanosomen. I. — Mitteilung : Das Phanomen der Trypanosomen-
wiederbclebung und das Vorhandensein vergarbarer Substanzen in den Lebern und deren
Extrakten, welcbe ‘ wiederbelebend * wirken. II. — Mitteilung ; Sind in den Extrakten,
welche aus den Lebern der an einer akuten Trypanosomiasis verendeten Tiere hcrgestellt
sind, noch durch Ilefe vergiirbare Substanzen vorhanden ? Centralbl. f. Bakt.., /, Or/g.,
96 , 356, 360.
(1928). Ueber die Stdrung des ZAickerstoffwcchsels bei Trypanosomiasen und Spirochatosen.
Biochem. Ztschr.j 193 , 264.
Schilling, Cl., and Rondoni, P. (1913). Ueber Trypanosomen-Toxlne und Immunitiit. Ztschr. f.
Immunitdtsf.j 18 , 651.
NOTES ON TREATMENT OF FIFTY-TWO
CASES OF RHODESIAN TRYPANOSOMIASIS
WITH BAYER 205 AND TRYPARSAMIDE
BY
GEORGE MACLEAN, M.B., Ch.B., D.T.M.
SLEEPING SICKNESS OFFICER, TANGANYIKA TERRITORY
{Received for puhlication, 14 May, 1929)
During the latter half of 1924 an outbreak of human Trypano-
somiasis was discovered in the Ufipa District of Tanganyika Territory,
and early in the following year cases were also found in the adjacent
District of Tabora.
The species of Tsetse present, G. morsitans, the acute nature
of the disease, a few months' duration only, and the finding of
‘ posterior-nuclear forms ' in a rat inoculated with the Ufipa strain,
all indicated that the disease was of the Rhodesian type.
Fifty-two cases (all of whom were diagnosed microscopically)
commenced treatment between November, 1924 and the end of
1925, and nearly all the survivors were kept under observation
until 1928.
In twenty-one cases injections of 10 to 14 grammes of ISayer
205 were given on the ist, loth, and 28th days respectively ; four
patients died before the second injection was due.
In three cases weekly injections of Bayer 205 were given.
Three cases were given Tryparsamide in 3-gramme doses weekly
for eight weeks.
The method of treatment subsequently adopted and administered
to twenty-five cases was to give a minimum of two injections of
Bayer 205, each of i gramme, followed after one or two months'
interval by twelve weekly injections of Tryparsamide. The first
two doses of Tryparsamide were usually 2 grammes, and after-
wards the dosage was gradually increased to 4 grammes ; there
was generally an interval of one month between the fourth and fifth,
and between the eighth and ninth injections. The drugs were
337
338
administered either intramuscularly or intravenously. Children
were generally given proportionately smaller doses.
Unfortunately it was difficult to get patients to attend regularly,
with the result that a large proportion did not receive treatment at
the specified time, and some did not receive the total dosage laid
down for them.
For the purposes of analysing the results of treatment the
following classification is adopted* : —
Class i. Comprises cases with no appreciable oedema or wasting
before treatment commenced. This Class consists almost entirely
of cases of less than six weeks duration and of ' carriers/ infected
persons with slight symptoms of insidious onset or no symptoms
at all.
Class 2. Comprises cases with appreciable oedema and wasting
before treatment, but who are still able to walk about and attend to
their ordinary wants.
Class 3. Comprises cases who are asthenic and emaciated and
too ill to attend to their ordinary wants.
The following are typical histories : —
Case U17. Female. Adult.
Condition before treatment : III about three months. Emaciated. Oedema
of legs and feet. Just able to walk. Trypanosomes found in the blood.
Treatment (First course) : Bayer 205, three injections intramuscularly in 1*2 to
i'3~gramme doses on 2.12.24, 12. 12. 24 and 29.12.24.
Total dosage 3*8 grammes.
Result : Apparent recovery for a time, but was again in indifferent health in
September, 1925.
Treatment (Second course) : Bayer 205, four injections in I -gramme doses
between 9.9.25 and 7.10.25.
Total dosage 4 grammes.
Result : Though improved, trypanosomes appeared again in the blood in December,
1925, and by February, 1926, there was a definite clinical relapse.
Treatment (Third course) : Bayer 205, three injections in i -gramme doses from
7.3.26 to 14.3.26.
Total dosage 3 grammes.
Result : Died 22.3.26.
* The cerebro-spinal fluid was not examined before treatment in any of these, cases but in the
routine examination of other series of cases it has hitherto been found that oi^ema is practically
never present except when the cerebro-spinal fluid i? infected.
m
Case U20, Female. Age about 30 years.
Condition before treatment : 111 about one month. No emaciation or oedema.
Able to walk about for miles. Trypanosomes present in the blood.
Treatment : Bayer 205, three injections intramuscularly in i*2-gramme doses on
2.12.24, 12.12.24, 29.12.24.
Total dosage 3*6 grammes.
Result ; Uninterrupted recovery. She was quite fit when seen in February, 1928.
Case T57. Male. Age about 25 years.
Condition before treatment : 111 one month. Emaciated. Oedema of feet.
Hardly able to walk. Trypanosomes present in the blood.
Treatment (First course) ; Bayer 205, three injections intravenously in i -gramme
doses between 12.9.25 and 27.9.25.
Total dosage 3 grammes.
Treatment (Second course) : Tryparsamide six injections in 3 to 4-gramme doses
from 27.10.25 to 18.12.25.
Total dosage 21 grammes.
Treatment (Third course) : Tryparsamide eight injections in 3-grammc doses,
from 1.5.26 to 3.7.26.
Total dosage 24 grammes.
Result : Recovery. No relapses. Was fit end of 1927. Not seen, but reported
to be fit, end of 1928.
Case T64. Female. Age about 25 years.
Condition before treatment : 111 three weeks. Emaciated. Oedema legs
and feet. Able to walk a little. Trypanosomes present in blood.
Treatment (First course) : Bayer 205, three injections in i-gramme doses from
7.10.25 to 21.10.25.
Total dosage 3 grammes
Treatment (Second course) : Tryparsamide, five injections in 3-gramme doses
from 7.11.25 to 18.12.25.
Total dosage 15 grammes.
Result : Improvement. Then relapse in April, 1926.
Treatment (Third course) : Tryparsamide, eight injections in 2 to 3-gramme doses.
Total dosage 20 grammes. .
Result ,: Died August, 1926.
340
The results obtained in the three classes are summarised in the
following tables : —
Tabi,*: I.
Showing cases which received a single injection of Bayer 205 only.
Category
Total
treated
Dead
Well
Class I
I
I
0
Class 2
I
' 0
■
Class 3
3
3
0
Table II.
Showing cases which received three injections of Ba)rer 205 over a period of 15 to 30 days and a total
amount of at least 3 grammes (children receiving proportionately smaller doses).
Category
Total
treated
Dead ^
I Alive
Relapsed
Well
Class I
8
3
0
5
Class 2
7
6
I
0
Class 3
2
, 2
0
0
Note. — Cases who were subsequently treated with Tryparsamide for relapse arc also included.
Table III.
Showing cases which received at least eight injections of Tryparsamide over a period of eight weeks
and a total amount of at least 24 grammes.
Category
Total
treated
Dead
1
Alive
Relapsed
Well
Class I
I
0
0
I
Class 2 1
2 i
1*
1
0
Class 3
0
i
0
0
0
• Died of pneumonia.
341
Tabli IV.
Showing cases which received at least three injections of Bayer 205; over a period of 15 to 30 days
and of a total amount of at least 3 grammes, followed within two months by a course of at least ten
injections of Tryparsamide and a total amount of at least 29 grammes (children receiving propor-
tionately smaller doses).
Category
Total
treated
Dead
Well
Class I
I
0
I
Class 2
4
3
r
Class 3
I
0
>
Table V.
Showing cases which received an incomplete course of Bayer 205 and Tryparsamide.
Category
Total
treated |
Dead
Alive
Relapsed
Well
Class I
1
*3
2
i
1 2
i
9
Class 2
4
I
1 I
2
Class 3
2
0 j
0
2
Table VI.
Showing relapsed or re-infected cases after further treatment.
Treatment after relapse
Died
Recovered
At least 3 grammes of Bayer 205 or Foumeau 309 in three or
more injections
5 *
0
Irregular course of Tryparsamide or Bayer and Tryparsamide
4
4
• Two of these cases, belonging to Class i, are not included in the preceding tables as they
received their first course of Bayer irregularly.
34 ;^
RESULTS OF TREATMENT
Before discussing the results obtained it is necessary to make
clear the position with regard to relapses. In none of the relapsed
cases could re-infection be excluded, and not until a large series
of treated cases is observed under fly-free conditions can data be
obtained which may distinguish the two conditions.
It may, nevertheless, be of significance that it is the late cases,
that usually ' relapse.' We may, perhaps, assume that re-infections,
if they have occurred, bear the same ratio to true relapses throughout
the three classes.
In general, the tables show that while early cases, Class i, treated
with Bayer 205 alone, have, in the majority of instances (over
60 per cent.) recovered, late cases (Classes 2 and 3) so treated,
almost invariably died, whereas equally late cases treated with both
Bayer and Tryparsamide have occasionally recovered..
The more advanced the cases before treatment, the greater the
tendency to relapse and death.
A relapse, when it occurs, usually becomes evident within less
than a year from the commencement of treatment, but may be as
late as fifteen months or more. There is no evidence yet that
relapses occur after two and a half years, but that they may do so
in some form or other is possible in view of the fact that, in cases of
apparent recovery, lumbar puncture performed nearly two years
after the commencement of treatment sometimes reveals a large
number of cells (as many as 260 per c.mm.) in the cerebro-spinal
fluid.
One point in connexion with relapses may be of practical
importance : namely, that parasites sometimes appear in the
peripheral blood when the patient feels in almost normal health
and is going about his ordinary duties. If these parasites are
infective these patients may be a greater danger to the community
than if they had been left untreated.
TOXIC EFFECTS OF THE DRUGS
Beyond the severe pyretic reaction that frequently follows the
first injection of Bayer 205, the only toxic S5miptoms seen afte*
this drug were Nephritis and a combination of Dermatitis and
Stomatitis.
343
It was not possible to make regular examinations of the urine
and some transitory albuminurias may have been overlooked.
Severe long-standing Nephritis was seen in only three cases, one of
whom, had Dermatitis. In two of these the Nephritis appeared to
be a contributory cause of death. Only one case of Dermatitis was
seen and it has already been described in a previous paper.
The only toxic effect of Tryparsamide seen was Optic Neuritis.
This was nearly always bilateral and usually complete and permanent,
though perhaps sometimes it may be partial and transitory. This
condition may possibly be due, not to the pure drug itself, but to
some product of its decomposition, for, though it occurs occasionally
when the solution is made in distilled water, it appears to be more
common if only filtered water is used, or if the solution is heated
to too high a temperature.
CONCLUSIONS
Generally speaking, the earlier the treatment the better the
chances of recovery. There is good reason to expect that an uncom-
plicated case taken in the first two or three weeks of infection will
make a complete recovery, if given four grammes of Bayer 205 in
three or four doses, the treatment being spread over a month. To
allow a margin of safety it may be advisable to administer as much
as eight grammes, but if this is done the urine should be watched
daily for albumen. How far Bayer 205 should be withheld when
albuminuria occurs is a matter for judgment in each individual case,
but generally the treatment should cease until the albumen disappears
if three grammes have already been given, but should not be withheld
for more than ten or fourteen days if only two grammes or less have
been given. An individual dose should not ordinarily exceed
one and a half grammes. The optimum total dosage of Bayer 205
is not known, and a series of late cases on a prolonged course of
treatment should be worth observing.
Tryparsamide alone, though not generally regarded as satisfactory
in this type of Sleeping Sickness, has given good results in some
cases and would seem to deserve further trial. Solutions of this
drug should always be made in distilled or freshly-collected rain
344
water, and the solution should not be allowed to stand long or heated
beyond blood heat. Should dimness of vision occur, treatment
should cease until the sight is completely restored.
Treatment by Bayer 205 followed by Tryparsamide gives better
results than Bayer 205 alone. When the combined treatment is
being given Bayer 205 should be administered in the same way
as when the drug is given alone and after this course Tryparsamide
should be given in 2 or 3-gramme doses at weekly intervals (with
or without a month’s interval between the fourth and fifth, and
the eighth and ninth injections) until at least 36 grammes are
given. What interval should elapse between the last dose of
Bayer 205 and the first dose of Tryparsamide is still a matter of
conjecture, but a month has been found suitable.
In the above series children generally reacted badly to treatment,
but this may pOvSsibly be because the doses were too ^mall. It has
since been found that children tolerate both drugs extremely well.
It is important that a series of treated cases who are in good
health but whose cerebro-spinal fluid remains abnormal for several
months after completing treatment, should be given a further course
of Tryparsamide without waiting tor the development of any
symptoms. These could then be compared in years to come with
cases that had not been so treated.
Work on the infectivity of Trypanosomes in relapsed cases is
urgently needed.
I am indebted to Drs. Buchanan, Park Noble, and Williamson,
and to Mr. Irvine, for completing the treatment in some of the cases
and for keeping them under observation ; to Dr. Coghlin, for
‘reporting on the Ufipa cases, in 1928.
I have to thank Dr. J. O. Shircore, C.M.G., Director of Medical
Services, Tanganyika Territory, for permission to publish the paper.
REFERENCE
Macjleam, G. (1928). A dermatitis associated with ^ Bayer 205' treatment of Rhodesian
Trypanosomiasis. Ann. *Irop. Med. Parasitol.^ S 2 ) 531*
THE ACTION OF PRAP. 3510 IN
RHODESIAN SLEEPING SICKNESS
BY
GEORGE MACLEAN, M.B., Ch.B., D.T.M.
SLEEPING SICKNESS OFFICER, TANGANYIKA TERRITORY
{Received for publication 14 May, 1929)
In 1928, supplies of a drug known under the name of Prap. 3510
were obtained in Tanganyika Territory, from the firm of
I. G. Farbenindustrie A. G., Hochst-am-Main, Germany. Prap. 3510
is a white powder easily soluble in cold water. It is an arsenic
compound but its formula is not disclosed.
The drug is made up in i, 2 and 2| gram ampoules, but there is
no other guide to dosage.
The first series consisted of three cases treated in April and May,
1928. Two of these were chosen because they were very advanced
cases for whom there was little hope of recovery with any known
treatment. The third case was comparatively robust. He was
regarded as a good subject because be appeared to have sufficient
reserve of vitality to react to Bayer 205 later if the new drug did not
prove efficacious. He was also suffering from Keratitis, and this
fact seemed an additional advantage in gauging the action of the drug.
The drug was not successful and all three patients eventually
died. This was to be expected in the first two, who could hardly
hope to recover unless the new drug proved more efficacious than
Bayer 205. The death of the third was rather a surprise and was
probably accelerated by the action of the drug.
The following is a brief history of each case : —
Case i. Male. Age about 30 years. Ill about 2j months. Condition on
the day treatment commenced : Just able to walk. Some emaciation but no
oedema. Auxiliary glands slightly enlarged. Fresh blood — Trypanosomes present
in fair numbers.
Treatment with Prap. 3510 ; 3*75 gms. intravenously.
First day after treatment : Vomited during the night. Fresh blood — No trypano-
somes in 150 fields, Cercbro-spinal fluid — Trypanosomes present. Cells
25 per c.mm.
345
346
Second day after treatment : Vomiting ceased. Fresh blood — No trypanosomes
in 1 50 fields.
Fourth day after treatment : Vomited again through the night. Fresh blood — No
trypanosomes in 200 fields.
Sixth day after treatment : Vomiting ceased during the previous day. Fresh
blood — No trypanosomes in 200 fields. Became rapidly weaker and died
in the afternoon.
Case 2. Male. Age about 40 years. Ill about 2 months. Condition
on the day of treatment : Just able to walk. Emaciated. Slight oedema of feet.
Epitrochlear glands enlarged. Fresh blood — Trypanosomes in large numbers.
Treatment with Prap. 3510 : 2*5 gms. intramuscularly.
First day after treatment : Vomited through the night. Fresh blood — No trypano-
somes in 200 fields. Cerebro-spinal fluid — Trypanosomes present. Cells
' 45. per c.mm.
Third day after treatment: Vomited yesterday. Weaker. Fresh blood — No
trypanosomes in 200 fields.
Fifth day after treatment : Vomiting ceased. Fresh blood — I^o trypanosomes in
200 fields.
Sixth day after treatment : Stuperose.
Seventh day after treatment : Comatose. Fresh blood — No trypanosomes in
200 fields.
Eighth day after treatment : Died.
Case 3. Male. Age about 20 years. Ill about 2| months. Condition
on the day of treatment : Well nourished. Able to walk for miles. No oedema.
Spleen, axillary and epitrochlear glands enlarged. Conjunctivitis and keratitis of
one eye. No vomiting. Fresh blood — Trypanosomes scanty.
Treatment with Prap. 3510 ; 2*25 gms. intramuscularly.
First day after treatment : Vomited the previous evening after the injection. Fresh
blood — No trypanosomes in fields. Cerebro-spinal fluid — Trypano-
somes present. Cells 150 per c.mm.
l^hd day after injection : No vomiting for 48 hours. Eye condition distinctly
improved. Fresh blood — No trypanosomes in 200 fields.
Sixth day after treatment ; No more vomiting. Conjunctivitis and keratitis almost
completely disappeared. Patient feels well. Fresh blood — Trypanosomes
numerous.
Seventh day after treatment : Fresh blood — Trypanosomes still numerous but arc
rather sluggish. After examination of the blood, 2 gms. of Pr 3 p. 3510 was
given intramuscularly. Vomiting set in shortly after administration but
was checked with Sodium Bicarbonate and Opium.
Eighth day after commencement of treatment : No vomiting, but weaker than
before second injection. Stained thick blood film — No trypanosomes.
Ninth day after commencement of treatment ; Weaker. Fresh blood — No trypano-
somes in 180 fields.
Tenth day after commencement of treatment ; Died.
347
The reactions observed in Case 3 suggested that the symptoms
following the administration of the drug might not be due to direct
action, but to the products of the sudden destruction of large numbers
of trypanosomes.
As the drug appeared to have a definite trypanosomicidal action,
it was decided that observations ought to be continued under modified
conditions. A fourth case was accordingly selected and i gm. of
Bayer 205 was administered to sterilise the peripheral blood.
A week after, 2 gms. of Prap. 3510 was administered intra-
venously. In this case there was little or no reaction, and the
patient was able to take eight weekly intravenous injections, a
total of 16 gms., without untoward symptoms and with very good
clinical results. Nine months after commencing these injections
he felt well except for some pains in his legs, and he was doing heavy
muscular work.
Two more cases were subsequently treated with Prap. 3510 alone :
at first, I gm. doses were given, but later the doses were increased
to 2 gms. These cases survived the treatment, but the results
were not satisfactory as the following histories show : —
Case 5. ATale. Age about 60 years. Ill about i inontli. Condition
on the first day of treatment : Fairly well nourished. Able to walk for miles.
Oedema legs and feet. Axillary and epitrochlear glands enlarged. Fresh blood —
Trypanosomes present in fair numbers. Cerebro-spinal fluid — Trypanosomes
present in fair numbers. Cells 30 per c.mm.
Treatment with Prap. 3510 : i gm. intravenously.
First day after treatment : No vomiting. Only symptom was a rise of temperature
about five hours after injection. Fresh blood — No trypanosomes in 1 50
fields. Stained thick film also negative.
Subsequent history of the case : The blood was again negative on the third and
twelfth days after treatment, and no untoward symptoms developed.
On the fourteenth day after commencement of treatment a second i gm.
dose of Prap. 3510 was given. 2 gms. were given on the twenty-first day,
2 on the twenty-eighth, and on the thirty-fifth.
Trypanosomes were present in the blood after the second and tliird
injections and in the cerebro-spinal fluid after the fifth.
No vomiting occurred even after the larger doses but the general
condition of the patient had not improved, and routine treatment with
Bayer 205 and Tryparsamide was resorted to.
Case 6. Male. Age about 25 years. Ill about 3 months. Condition
on the first day of treatment : Nutrition and general health good. I'race of oedema
of legs and feet. Able to do a moderate amount of work. Blood (frcsli and
34 ^
Stained) — no parasites seen. Cerebro-spinal fluid — Trypanosomes (70 per c.mm.)
present. Cells 5 per c.mm.
Treatment with Prap. 3510 : I gm. intravenously.
First day after treatment ; No vomiting. Stained thick blood film — No trypano-
somes.
Subsequent history of the case : Trypanosomes were found in the blood twelve days
after treatment, but no untoward symptoms developed.
On the fourteenth day after commencement of treatment a second
I gm. dose of Prap. 3510 was given, 2 gms. were given on the twenty-first
day, 2 on the twenty-eighth, and on the thirty-fifth.
Trypanosomes were present in the blood after the second and third
injections, and in the cerebro-spinal fluid after the fifth.
During the first month of treatment there was a slight improvement
in the general health, but after the fifth injection, patient began to lose
ground rapidly, and it became necessary to revert to Bayer 205 treatment.
There was no vomiting after the larger doses of Prap. 3510,
CONCLUSIONS
The limits of the pharmacological dose of Prap, 3510 in man are
not known, but there is reason to suspect that its action is much
more toxic if there are large numbers of trypanosomes in. the
peripheral circulation when it is administered.
It has proved much less efficacious than either Bayer 205 or
Tryparsamide in moderate doses. While it may possibly be an
efficient trypanosomicide in larger doses the margin of safety is
so narrow that it is of no practical value when administered alone.
Its action in association with Bayer 205 is being observed, but it will
probably take some years before any definite conclusions can be
arrived at about this method of treatment.
The drug is well worth a trial in the various trypanosomiases
of domestic stock.
I am indebted to Dr. Fairbaim for keeping Cases 5 and 6 under
supervision during the latter part of their treatment.
I have to thank Dr. J. O. Shircore, C.M.G., Director of Medical
Services, Tanganyika Territory, for permission to publish the paper.
AN ACCOUNT OF THE ANATOMY OF
CERTAIN CESTODES BELONGING TO THE
GENERA STILESIA AND AVITELLINA
BY
H. F. NAGATY
{yeterinary Research Student in the Parasitology Department of the
Liverpool School of Tropical Medicine)
{Received for publication 31 July, 1929)
Plate V
INTRODUCTION
In the museum of the Liverpool School of Tropical Medicine
there is a large collection of cestodes referable to the sub-family
Avitellininak. The bulk of the material was collected from Africa.
Investigations on these worms were suggested by Dr. r.
Southwell, F.R.S.E,, of the Liverpool School of Tropical Medicine,
to whom I am also indebted for much help and criticism. I am
also indebted to Professor W. Yorke, M.D., for much valuable advice
and help.
The material was preserved in formalin solution and was all
fragmented, no complete worms being present and, owing to this
fact, it proved a laborious task to follow the* development and
relationships of the different organs in the species described.
A large number of total mounts, serial, transverse, horizontal
and sagittal sections of the different parts of the worms were made.
The thickness of the sections varied according to circumstances,
from 5/^ to 25^. The stain used throughout the work was acetic
acid alum-carmine.
As many camera lucida drawings as possible were made because,
in my opinion, this is the surest and easiest means of identifying
these worms. Furthermore, the preparation of these figures assisted
materially in the elucidation of several points which were not at first
perfectly clear.
349
350
Family Anoplocephalidae Fuhrmann, 1907.
Scolex unarmed, without rostellum or accessory suckers.
Segments broader than long. Genital organs single or double in each
segment. Genital pores may be absent. Genital ducts generally
pass dorsally to the excretory vessels, but may pass between them
or ventrally to them. Testes numerous or few. Uterus tubular,
reticulate or sac-like ; it may become transformed into egg-capsules,
or it may be replaced by one or more paruterine organs. Eggs with
three envelopes, the inner one being chitinous and sometimes bearing
a pyriform apparatus. Adults in birds, mammals and reptiles. In
no species of this family is the life-history known.
Type genus : — Anoplocephala Blanchard, 1841.
Key to Sub-Families (after Southwell).
Uterus persistent Anoplocephalinae
Uterus developing paruterine organs Ihysanosominae
Uterus breaks up into egg capsules Linstowinae
Sub-family Thysanosominae Fuhrmann, 1907.
Large worms. Genital pores double or single ; in the latter
case they are irregularly alternate. Genital canals dorsal to excretory
vessels or between them. Testes very numerous or few, in a single
field, or in two lateral groups. Female genitalia in poral half of
segment. Vitelhne gland may be absent, in which case the ovary
contains the nutritive cells. Uterus tubular, sometimes very long,
and undulating. Paruterine organs present ; may be very numerous
or single. They each contain several eggs. Adults in ruminants.
Type genus : — Thysanosoma Diesing, 1835.
Key to the Genera included in the Sub-Family Thysanosominae
(after Southwell).
With a double set of genital organs in each segment thysanosoma
With a single set of genital organs in each segment I
1. With one paruterine organ in each segment Avitellina
With more than one paruterine organ in each segment 2
2. With two paruterine organs in each segment Stilesia
With numerous paruterine organs in each segment 3
3. Testes within excretory vessel Ascotaenia
Testes in two fields, one lateral, 10 the excretory vessels on each
side Helictometra
351
Baer (1927) united the sub-family Avitellininae Gough, 1911,
with the sub-family Thysanosominae Fuhrmann, 1907.
The following genera referable to this old sub-family
Avitellininae have been described, viz,, Stilesia Railliet, 1893,
Avitellina Gough, 1911, Hexastichorchis Blei, 1921, and Anootypus
Woodland, 1928.
Southwell (1929) considered that only two genera are valid, viz.,
Stilesia and Avitellina, and he placed the genera Hexastichorchis and
Anootypus as synonyms of the genus Avitellina. This paper deals
with species of the two genera Stilesia and Avitellina.
Diagnosis of the genus Stilesia Railliet, 1893.
Strobila thin and narrow. Outer segmentation always distinct,
and corresponding to the internal segmentation of the genitalia.
Longitudinal muscles in one layer. Ventral excretory vessels lateral
to dorsal vessels. Testes in two groups, one on each side of the
strobila, all external to the dorsal excretory vessels, none in the
middle field. Cirrus sacs ventral and anterior to the vulvae.
Genital ducts pass between the excretory vessels and dorsal to the
nerve. Ovary single, situated porally, internally to the ventral
and externally to the dorsal excretory vessels. Uterus single
but with two lateral dilatations, each situated between the dorsal
and the ventral excretory vessels. Paruterine organs double, and
taking the place of the lateral dilatations of the uteri. Parasites in
ruminants.
Type species : — Stilesia glohipunctata (Rivolta, 1874), Railliet,
1893.
Key to the Known Species of the Genus Stilesia.
Testes all lateral to the dorsal excretory vessels S. hefatica
Testes all lateral to the ventral excretory vessels I
Vas deferens forms a mass of intricate convolutions between the
cirrus pouch and the outer wall of the ventral excretory vessels. . . .9. vittata
Vas deferens forms three or four close coils before it enters the
cirrus pouch 5. glohipunctata
Diagnosis of the genus Avitellina Gough, 1911.
Strobila thin and narrow. Outer segmentation usually not
distinct. Longitudinal muscles in a single layer in the cortex and
well developed ; another thin subcuticular layer may or may not be
352
present. Testes in two or four rows. Uterus and paruterine
organs single in each segment. Genital ducts pass dorsal to the
excretory vessels and nerve.
Type species: — A. centripunctata (Rivolta), 1874, Railliet, 1893.
Key to the Species of the Genus Avitellina,
Dorsal excretory vessels completely absent i
Dorsal excretory vessels present 2
1. With four rows of testes A. edijontaina
Woodland, 1928
With two rows of testes A. ricardin
Woodland, 1928
2. Dorsal excretory vessels lateral to ventral excretory vessels ... 3
Dorsal excretory vessels median to ventral excretory vessels ... 4
3. Some testes lateral to the dorsal excretory vessels A. pintneri
Blei, 1921
No testes lateral to the dorsal excretory vessels A. ctgyptiaca n.sp.
4. Outer row of testes one testis deep 5
Outer row of testes more than one testis deep 6
5. Mature paruterine organs kidney-shaped A. sudanea
Immature paruterine organs snail-shaped A. lahorea
Woodland, 1927
6. Outer rows of testes are four to eight deep, and there is a
distinct row of testes external to the nerve cords A. southzvellin.s'p.
Outer rows of testes three to six deep ; paruterine organs arc
like bunches of bananas 4, goughi *
* Woodland, 1927
Outer rows of testes are two to three deep and with anterior
annular thickenings on each proglottid A. chalmersi
Woodland, 1927
Outer rows of testes one to two deep ; paruterine organs
sac-like A. centripunctata
(i) Stilesia glohipunctata (Rivolta), 1874, Railliet, 1893.
Host : — Ovis laticauda.
Locality : — Unknown, probably Africa.
The worms are whitish in colour and delicate. The margins
are serrated on account of the fact that the posterior angles of the
segments project laterally, thus distinguishing the anterior from
the posterior ends of the pieces of the strobila with certainty. The
breadth of the immature parts of the strobila is about 330/^. The
individual segments are about 8o/^ to 90 in length. The male
mature strobila measure about 864^ in breadth and the individual
segments 144, w to 196/1 in length. In the region where the paruterine
organs are well developed, the breadth of the worm varies from
490/A to 900// and the segments are about 220/^ in length in the
narrow parts, and about iio/i in length in the broader parts. The
genital pores are irregularly alternate and open near the anterior
angles of each segmmt.
353
Excretory System. Both excretory vessels are well developed
throughout the whole length of the strobila. The ventral vessels
are lateral to the dorsal vessels and measure, in the immature region,
about TOfji in diameter. The dorsal vessels have thicker walls
than the ventral ones and are smaller, measuring only y ft in diameter ;
they lie slightly dorsal to the ventral vessels.
In the male mature region, however, the ventral vessels enlarge
to about 30/>e and the dorsal vessels to about lo/^, in diameter. In
the region where the paruterine organs are developed, the ventral
vessels measure about 40/^ and the dorsal vessels only 6/z in diameter,
but the latter are quite distinct.
Muscular System. The longitudinal muscles are in one layer
and are feebly developed except in the anterior part of the worm,
where they are well developed.
Male Genitalia. The testes are situated lateral to the ventral
excretory vessels. They are more or less restricted to the angles
formed by the ventral excretory vessels and the posterior borders of
the segments. There are from four to seven on each side.
Porally they are always posterior to both the cirrus pouch and
the vulva, and they never occur anterior to these organs. The testes
on the aporal side usually out-nnmber those on the poral side.
Each fully mature testis measures about 47// in diameter.
The cirrus pouch is pyriform and measures 54// by 43// ; it is
always anterior and ventral to the vulva.
The vas deferens is thrown into three or four coils before it enters
the cirrus pouch.
Female Genitalia. The ovary is situated between the dorsal
and ventral excretory vessels on the poral side, and at first is indicated
by a cluster of darkly-staining nuclei. It measures about 58/i by 43//
when fully mature.
Immediately posterior to it is another cluster of darkly-
staining nuclei indicating the rudiments of the poral part of the
uterus, and in the corresponding position in the aporal half of the
segment a similar uterine rudiifient is present. Each of these
measures about 25// in diameter. Later on the uterus becomes a
spherical or oval mass of fibres measuring about 35/>e in diameter and
yet containing no eggs.
In the segments immediately posterior a very interesting
354
phenomenon is displayed, in that the two uteri enlarge at the expense
of the ovary. That is to say, in the succeeding twenty to fifty
segments the ovary gradually atrophies, the two uteri enlarge and
finally contain the eggs, the ovary having completely disappeared.
The eggs can be seen passing from the ovarj^ to the poral part of the
uterus, which latter lies posteriorly and in close contact with it. No
connecting duct was seen between them : the eggs most probably
pass through the tissues. In several segments eggs were seen
wandering towards the aporal parts of the uteri and a few of them were
distinctly amoeboid in shape. In some cases the duct connecting
the two parts of the uterus was seen containing the wandering ova ;
in other cases, however, it could not be traced although eggs were
seen in the middle of the segments. This duct is tortuous in its
course, appears to be contractile and measures about 5/i only in
the region where there are no ova. The writer must state here that
the figures 8 and lo oi Stilesia vittata and Stilesia ' glohipunctata in
Gough’s monograph are erroneous with regard to the position and
relation of the uteri to the ovaries. He figures the uteri anterior
and median to the ovaries, but they are without doubt immediately
posterior to them, as shown in fig. 2 .
Paruterine Organs. In partly-gravid strobila the paruterine
organs are situated between the dorsal and ventral excretory vessels
and are attached posteriorly to fibrous structures, which latter
assume two shapes, one being like the letter T and the other
resembling an inverted letter L. The short limb of the L-shaped
fibrous structure is directed inwardly. If we trace these structures
posteriorly, we find that the cross-bar of the T-shaped rudiment
or the short limb of the L gradually expands and separates from
the [remaining limb of the T or the long limb of the L, forming a
strong fibrous pad in front of the paruterine pouch to be described.
The ^remaining Hmb of the T or the long limb of the L develops,
and a membrane round the fibres is differentiated, forming in the
end the paruterine pouch. This is situated anteriprly and somewhat
median to the paruterine organ and is composed of concentrically
arranged fibres. An opening between this pouch and the paruterine
organ is present and through it some of the fibrous tissue passes
into the paruternie organ, pushing the eggs towards its posterior
margin. In some paruterine pouches, especially those at the posterior
355
end, a number of eggs, two or three, can be seen in the middle of the
concentric fibres.
The paruterine organ also changes its position from being
median to the ventral excretory vessel to being dorsal, or even
completely external to it in some segments ; being pushed, so to
speak, by the developing paruterine pouch, which, so far as can be
seen, is located between the dorsal and the ventral excretory vessels.
Stiles, in his description of Stilesia glohipunctata, says : — ' An
organ, the function of which I am unable to explain, appears anterior
to the uteri and running transversely. This organ lies ventrally of
the vas deferens — in those cases where the vas deferens extends
so near the anterior margin and stains quite dark in carmine or
haematoxylin.* I am of opinion that these organs are the fibrous
pads referred to in this paper.
(2) Stilesia vittata Railliet, 1896.
Host : — Camelus sp. (Camel).
Locality : — Unknown.
The strobila to the naked eye appears quite different from that
of Stilesia hepatica. It is more transparent and less fleshy. Seg-
mentation is visible to the naked eye.
The fragments examined measure up to 10 cm. in length and
from 2*5 mm. to 4 mm. in breadth. All the segments are broader
than long, and measure about 215// in length.
The fragments are from different parts of the strobila and nearly
all of them are folded ventrally on themselves and much curled and
twisted.
Strong fibrous pads are situated towards the anterior edges of
gravid segments ; each pad is composed of a middle part and two
denser, saucer-shaped extremities, the concavities of which are
directed posteriorly, covering the inner parts of the paruterine
organs. The genital pores are irregularly alternate and open near
the anterior angles of the segments.
Excretory System, The ventral excretory vessels are well
developed, especially in the posterior parts of the strobila, where
they measure about 214/^ in diameter, whilst anteriorly they measure
about 73/i.
The dorsal vessels, on the other hand, are only well developed
in the anterior part of the worm, and measure about 23 /« in diameter
and have thick walls. They are situated internally to the ventral
excretory vessels, and either slightly dorsal to them or at the same
level.
Posteriorly the dorsal vessels gradually atrophy and the ventral
enlarge.
In each segment there arise from the outer and inner sides of both
ventral vessels, two small, thin-walled tubes, having a diameter of
about 7^. Each arises either singly or as the result of the fusion of
two small ducts. The internal branch joins the main ventral
vessel on the other side, being situated towards the posterior margin
of the segment. The outer branch can be traced towards the margin
of the se^ents where it divides into three or four branches. Like
the internal branch it is situated near the posterior margin of the
segment.
Nervous System, The nerve cord is situated about midway
between the lateral margin of the strobila and the outer wall of the
ventral excretory vessel.
Muscular System. The longitudinal muscles are in one layer
only, not in two as described by Gough. This layer is very weakly
developed. A subcuticular layer is not present. The transverse
muscles are also feebly developed and separate the denser, cortical
parenchyma from the spongy medulla. Strong and distinct muscular
fibres run from the wall of the genital atrium to the dorsal and ventral
surfaces of the segment, and ramify before reaching the ventral or
dorsal surfaces. They are undoubtedly modified dorso-ventral
fibres.
Calcareous Corpuscles are irregularly scattered throughout the
parenchyma but tend to be clustered towards the junction of the
segments, more so towards the margins. In cross-sections they
are seen to be situated mostly in the Cortical parenchyma. They
stain very lightly and most of them show a concentric structure.
They are irregular in shape and measure from 7 fJi to lo/e.
Male Genitalia. The testes are spherical or oval in shape and
are situated externally to the ventral excretory vessels. There
are from five to ten on each side, each measuring about 66/i in
diameter. On account of the fact that the male and female ,genital
ducts occupy the anterior half of the Segment on the poral side,
357
the testes of this side are situated in the posterior half, whilst on
the aporal side they extend much more anteriorly. It is noteworthy
that the testes have not atrophied even in segments in which the
paruterine organs are well developed. I'he vas deferens, which has
not previously been described, is clearly shown in our toto mounts.
It begins on the aporal side as a thin tube having a diameter of about
7//. It appears to arise from the innermost testis of the aporal side
and runs across the anterior part of the segment, in front of the
vessel connecting the two ventral excretory vessels. In the middle
field it is very convoluted and stains more deeply than the rest of the
duct, thus making this part easily seen even under a low
magnification. More laterally towards the pore side it again con-
tinues its more or less straight course. It crosses the posterior
margin of the poral paruterine organ and then bends towards the
anterior margin in front of the testes, forming a mass of intricate
convolutions, before it enters the cirrus pouch, i.e., between the
pouch and the outer wall of the ventral excretory vessel. As far as
can be seen there is no capsule surrounding this mass of convolutions.
Immediately internal to this mass of convolutions the vas deferens
dilates into a small oval vesicula seminalis with thick walls, the
contents of which stain deeply — these are probably spermatozoa.
The vas deferens could only be seen in a few segments ; the middle
convoluted part is, however, visible in many others. 1'he cirrus
pouches are oval in shape and open towards the anterior angles
of the segments. They measure about 115// by 66//. The cirrus
was protruded in some of the segments and measured about 83//, in
length.
Female Genitalia. The ovary is only found in segments where
the paruterine organs are not yet developed. It is situated on the
poral side only, between the ventral and dorsal excretory vessels
but nearer the former. It measures about loo/i by 66^ and contains
from twenty to thirty ova.
The vulvae measure about 82/i by 13/y. and are dorsal and posterior
to the cirrus pouches on both sides.
The genital atria are about 66// in depth and their walls are
covered by long, slender, hair-like processes which measure about
33// in length. The genital pores open in the centre of a conspicuous
papilla which is elevated from the surface of the margins.
358
The uterus consists of two dilated lateral parts, one on each
side, which are situated between the dorsal and ventral excretory
vessels. There can be no doubt that these two dilatations are
connected by a duct similar to that found in Stilesia hepatica and
Stilesia globipunctata, but unfortunately it could not be traced in our
specimens, in spite of the fact that many transverse sections were
made in different regions of the strobila. Paruterine organs take
the place of the uteri in posterior segments : there are two in each
segment, one internally to each ventral excretory vessel and in
close apposition to its internal wall.
(3) Stilesia hepatica Wolffhugel, 1903.
Host Cobus cob, gall bladder and bile ducts ; East shore,
Lake Albeit, Tonya, Africa ; (2) Liver of sheep, Durban, South
Africa ; (3) Hepatic duct of sheep, Rhodesia.
The breadth of the fragments range from 1*3 mm. to 2*4 mm.
Segmenjtation is quite distinct to the naked eye. The margins of the
strobila are serrated on account of the projection of the posterior
angles of the .Segments. The latter are much shorter than broad,
measuring from about in male mature segments, up to zoo/Lt in
length in gravid segments. The posterior borders of most of the
segments are excavated, forming shallow concavities into which the
anterior borders of the succeeding segments lie.
The genital pores- are irregularly alternate and situated near
the middle of the lateral margin of the segments.
Excretory System, The excretory vessels are both well developed ;
the ventral ones are situated externally and ventrally to the dorsals
and are about 66/^ in diameter. The dorsal vessels have thicker
walls than the ventral ones and they measure about 40// in diameter.
In no other species of the genus Stilesia are the dorsal vessels so well
developed and constant, or are the walls so thick.
Nervous System, The nerve cord is situated externally to
the ventral excretory vessels and is nearly midway between the
margin and the outer border of the ventral vessel.
Muscular System. The longitudinal muscles consist of a stout
layer which almost surrounds the strobila. It is situated about
132/i below the cuticle and measures about 99/^ in thickness.
Male Genitalia, The testes are oval in shape, measuring about
359
ixbfji by 46^ in diameter when fully mature. They are arranged
in two rows, one on each side of each segment. From eight to ten
testes can be counted on each side. They are situated laterally to the
dorsal excretory vessels and dorsally to the ventral vessels.
The vas deferens from the aporal testes meets that from the poral
testes, forming by their union the main vas deferens. This passes
towards the poral side between the two excretory vessels and dorsal
to the nerve. It forms a few loops dorsally to the ventral excretory
vessel before it enters the cirrus pouch. The latter is pear-shaped,
measuring 83/^ in length by 50// in maximum diameter.
Female Genitalia. The ovary is spherical or kidney-shaped
and measures Sou by 50//. It is situated porally just median to the
ventral vessel and nearly on the same level. It lies laterally and
ventrally to the dorsal vessel. The uterus is single but consists of a
transverse tube dilated at each extremity ; each dilatation is oval,
measures 66^ by 50//, and is situated between the dorsal and the
ventral excretory vessel on each side. The two parts arc connected
by a duct through which ova travel from the poral to the aporal
parts of the uterus. The paruterine organs arc two in number, one
on each side, and they measure about 132/f by loo//.
(4) Avitellina centripunctaiq (Rivolta), 1874, Kailliet, 1893.
Host : — Ox.
I.ocality : — Freetown, West Africa.
The fragments examined measure about 2*5 mm. in breadth. The
margins appear slightly serrated, but when the fragments are suitably
magnified, these indentations are found not to correspond to the
segments, as two or three genital openings may occur between two
indentations. This is the case in the male mature segments, but in
the gravid ones the indentations are not so deep and the margins are
only raised here and there, especially where the genital pores open.
With regard to Woodland's statements that ‘ in gravid proglottids
of A. centripunciata the margins are more salient posteriorly and
are crenulated on their anterior .borders,' and (in a footnote),
' curiously enough, Gough's figure of the Transvaal species described
by him shows crenulations on the posterior border of the margin,* it is
to be noted that our specimens do not show these characteristics of
the margins described by Woodland and Gough. The genital
360
pores are irregularly alternate, and the segments are very short ;
in male mature and gravid segments there are no septa formed
between the segments, although Woodland figures them. In gravid
segments, however, strong fibrous pads, which stain deeply, are
formed in front of the paruterine organs.
Excretory System. This is composed of four longitudinal vessels,
two on each side. The external pair, the so-called ventral vessels,
are large, and can be seen with the naked eye, as two clear lines in
stained total mounts. Each measures, in cross-section, about
120/ji by 50// in the male mature region, and 200/4 by 150/^ in the
gravid region, and they have thin walls. The internal pair, the
so-called dorsal vessels, are very small in comparison with the ventral
ones, and can only be seen under high magnification. In transverse
sections they are rendered conspicuous by the presence of clusters of
nuclei, which surround them. Attention is here drawn to the
position of these so-called dorsal vessels ; they are, 'in fact, placed
ventrally. In order to determine which was the dorsal and which
was the ventral surfaces, the writer has always relied on the position
of the ovary as being ventrally placed, and on the passage of
the genital ducts dorsal ly to the excretory vessels and nerve. In
male mature strobila the dorsal vessel can be seen under high
magnification and is situated about. 80/4 internally to the inner wall
of the ventral vessel. In gravid strobila, however, the vessel is very
minute, and is situated a distance of about 60/4 internally to the
inner wall of the ventral vessel, the difference between the two
distances being evidently due to the enlargement of the ventral
excretory vessels.
Nervous System. This consists of two nerve cords, one external
to each ventral excretory vessel, and at one-third the distance from
the external wall of the latter vessel and the lateral margin of the
strobila.
Muscular System. This consists of an inner thick and an outer
thin layer. The former is about 40/4 in thickness and is situated
about 80/4 from the cuticle. It surrounds the strobila except for two
gaps at the lateral margins of the worm. The fibres are arranged in
pyramid-shaped groups, whose summits are directed outwards.
The outer layer is situated under the sub-cuticula, and is one fibre
thick..
Male Genitalia. The testes are arranged in four rows, one on
each side of each of the ventral excretory vessels. The outer row is
one or two testes deep, and does not extend laterally beyond the
nerve cord. The inner one is four to five testes deep. The testes
are spherical, and have a diameter of about 66//. The cirrus pouch
is pyriform, much shorter than the vagina, and measures about
115^ by 50^ ; it is always anterior to it.
Female Genitalia. The ovaries are spherical in shape, and form
two rows in the strobila, one on each side of the medianly-placed
uteri. Each ovary measures about 50// and is situated slightly behind
and ventrally to the poral side of the uterus of the same segment.
The vulva is spindle-shaped, and covered by gland cells, which,
in surface view, gives it the appearance of a mulberry. It measures
about 2 i6^u in length, by 43// in breadth, and is always situated
posteriorly to the cirrus pouch, but it may be cither dorsal or ventral
to it.
The vagina passes dorsally to both excretory vessels and
nerve ; it dilates into a receptaculum seminis, midway between the
inner wall of the ventral excretory vessel, and the lateral margin of
the uterus. It is spindle-shaped, measuring 173// by 72// and is
often full of spermatozoa. Immediately internal to it, the vagina
divides into an oviduct which runs to the posteriorly-situated ovary,
and a uterine duct which runs to the uterus ; both these ducts
have thicker walls than the vagina.
The ovaries and testes atrophy as soon as the paruterine organs
develop, the former first.
The uteri and paruterine organs are almost in one row in the
middle field of the strobila, but are situated .slightly on the poral .side.
Fibrous pads are yet not developed in front of the paruterine organs in
this region. Later on, the uteri become enlarged, sac-like and
contain the eggs, but in our specimens no capsules were seen round
the latter.
More posteriorly, strong fibrpus pads are formed in front of each
paruterine organ. These are curved rods of tissue, the concavities
of which are directed posteriorly. In the middle of this concavity
there lies an oval fibrous organ, the paruterine pouch which measures
about 162 fjL by 108^.
362
(5) Avitellina sudaneaV^ooiMdJid, 1927.
Host : — Ovis laticauda.
Locality : — Unknown ; but the geographical distribution of this
host is Tartary, Arabia, Persia, Barbary, Syria and Egypt. These
worms were probably collected in Egypt.
The fragments examined range in size from i cm. to about
15 cm. in length, by about 2 mm. in breadth. Externally the
strobila do not appear to be segmented ; when suitably magnified,
the genitalia definitely indicate true segmentation. In the male
mature region, the margins of the worm are not indented segmentally,
nor are there fibrous septa between the segments ; the latter, however,
develop in the gravid part of the strobila.
The genital potes are irregularly alternate.
-Excretory System. The ventral vessels appear as comparatively
clear, wide canals on each side, and in the immature region they
measure about 50/^. The dorsal vessels have a diameter of about
26/^ and are situated internally to the former. In a male mature
strobila measuring 1*25 mm. in breadth, the ventral vessels are
well developed, thin walled, and have a diameter of 80//. In a
gravid strobila they attain a diameter of 250//, while the dorsals
measure only about 4// in diameter. Thus, antero-posteriorly the
ventral vessels enlarge, whilst the dorsal ones become smaller.
Muscular System. The longitudinal muscles are apparently
in a single layer. No trace of the outer layer described by Woodland
could be found in the specimens examined.
Male Genitalia. The testes are arranged in four rows, one on
each side of each of the ventral excretory vessels. The external
row is one testis deep, and in the male mature strobila is very much
interrupted ; thus in a piece of strobila containing 41 segments,
there are, on one side, 19 testes external to the ventral vessels and
84, internal to it. On the other side there are 15 testes external
to the ventral vessel and loi internal to it. It will thus be noted
that the outer row of testes is absent in many segments ; in the
gravid region, however, it is more continuous. The internal row is
two to three testes deep.
Each testis is oval or spherical and measures about 90/* by 6o/<
in diameter. The vas deferens can be traced tp the level of the
363
ovary and is thrown into a few convolutions. The cirrus pouch
is pyriform, about the same length as the vulva, or slightly shorter,
and measures 115// by 36;^^. It contains several coils of the vas
deferens, which in the gravid segments occupies the entire cirrus
pouch. The latter extends to about three-quarters the distance
between the lateral margins and the outer wall of the ventral
excretory vessel.
Female Genitalia. The ovary is kidney-shaped. In male mature
segments it is situated on the poral side of the rudiment of the
paruterine organs ; it measures about 80 u by 66/^.
The vulva is pyriform and covered, except at its extreme distal
extremity, by a layer of glandular cells. These — the minute structure
of which can only be seen with an oil immersion lens — are club-
shaped, their distal ends being dilated, and each contains a single
nucleus.
The vulva measures about 1 30// in length, by 40/i in breadth, with
the layer of gland cells included, but I9/^ only excluding the layer
of gland cells.
The vagina is also covered by similar cells, throughout its length,
except in the region of the reccptaculum seminis ; the latter is
spindle-shaped, measures about 8o/.« by 32//,, and is situated
immediately median to the ventral excretory vessel. In the gravid
strobila it enlarges, and becomes globular, having a diameter of
about loo/f ; the glandular cells disappear and it becomes almost
filled with spermatozoa. Internally to it, the vagina divides into an
oviduct leading to the ovary, and a uterine duct running to tlie
uterus. These two tubes are wider than the vagina.
The vulva is usually posterior to the cirrus pouch in almost
all the segments, but is rarely anterior or on the same dorso-ventral
plane. Thus, in 150 segments, the vulvae were posterior except
in four cases, where they were anterior, and nine cases in the same
dorso-ventral plane as the cirrus pouches. The vulvae, again in the
majority of the segments, are dorsal to the cirrus pouches ; in some
they are ventral.
The paruterine organs in this species are of a peculiar shape, as
shown in the figures, and anterior to each is an inter-segmental
fibrous pad, which stains deeply. Each paruterine organ measures
132/^ by 66/«. The eggs are spherical, and measure 23/^ in diameter.
3^4
(6) AvitelUna southwelli, n.sp.
Host : — Sheep.
Localit}^ : — Accra, West Africa.
The fragments examined vdivy in length from lo cm. to 50 cm.,
and have a breadth of about 3*2 mm. in the male mature region.
The worm is fleshy compared with other species of this genus and,
in the gravid region it is almost cylindrical.
In total mounts the lines of segmentation in the male mature
region are, at first, very difficult to detect, as there are no septa
between them. The genital organs are so crowded together that
it was thought in the first instance that each segment contained
two oyaries. Close examination by means of horizontal and trans-
verse sections showed, however, that the segments are very short,
and contain only one ovary which is situated on the poral side of the
uteri.
In gravid strobila, however, the segments are longer, measuring
about 72^ in length and indistinct septa are formed between them,
which are only visible when horizontal sections are made.
Excretory System. This is composed of the usual pairs of large
ventral vessel and the small internally situated dorsal vessels.
The former are wide, measuring about 240// in the male mature
region and about 320/^ in the gravid region. They follow a very
tortuous course. Entire groups of encapsuled eggs, as well as
isolated ones liberated from their capsules, are seen inside the
ventral vessels in the gravid segments. The dorsal vessels measure
about 7 fJL in the male mature region. They are completely atrophied
in the gravid strobila.
Muscular System. The longitudinal muscles are in one layer
which is well developed and consists of separate bundles of about
twenty fibres each.
Nervous System. This consists of two longitudinal nerves situated
one on either side, about midway between the lateral margins of the
worm and the outer walls of the ventral excretory vessels.
Male Genitalia. The testes are numerous, compared with other
species of this genus ; they are spherical and measure from 50/i to
8o/<, being arranged in four rows^, one on each side of the ventral
excretory vessels. The outer row is four to eight testes deep and
3^5
there is a distinct row one testis deep external to the nerve cord.
This condition, i.e., the presence of testes externally to the nerve cord
and of the large number of testes externally to the ventral excretory
vessels, has not been described before in any species of the genus
Avitellina, and, together with other peculiarities to be discussed
later, justifies the erection of a new species. The internal row is
four to six testes deep and extends from the internal wall of the
ventral excretory vessel to the region of the ovaries.
The vas deferens is loosely coiled before it enters the cirrus
pouch and runs dorsally to both the excretory vessels and the nerve.
The cirrus pouch is pear-shaped and contains several coils of the
vas deferens ; it measures about 144// by 36//.
Female Genitalia. The ovaries are in two longitudinal rows
immediately median to the internal row of testes, and in each row
they are situated close to each other. Between these two rows are
the uteri. As the latter develop the essential genital organs atrophy,
the ovaries first.
Each ovary is situated ventrally and internally to the dorsal
excretory vessel close to the poral end of the uterus. It is distinctly
oval, measuring 70/x by 50/i. Leading from the ovary is a short
oviduct which unites with the uterine duct and forms the ootype or
fertihzation canal. Externally to the latter the vagina dilates to
form a receptaculum seminis which is situated dorsally, midway
between the dorsal excretory vessel and the poral extremity of the
uterus ; it is spindle-shaped and measures about 65// by 36/^.
The vulva is elongated and surrounded by glandular cells ; it
measures 200/^ by ii^a, tapering towards both ends and passing
gradually into the vagina.
The genital ducts pass dorsally to both the excretory vessels
and the nerve.
The vulva is situated either dorsally or ventrally to the cirrus
pouch, and they are on the same plane dorso-ventrally. The uteri
lie in the middle fifth in the male mature strobila and the middle
third in gravid strobila. At first *they are narrow transverse bands
of tissue which alternate markedly from side to side. Posteriorly
they become sac-like and disposed in two longitudinal rows.
Eventually they enlarge laterally and become pear-shaped. When
fully gravid they occupy the whole region between the inner walls
of the ventral excretory vessels. Mature paruterine organs measure
about 326// in length by 2i2/i in maximum breadth, and each contain
from three to four egg capsules. The egg measures about 2,2 fji in
diameter. This worm differs from all hitherto described species of the
genus Aviiellina in the following points : —
(1) The outer row of testes is from four to eight deep and there
is a row, one testis deep, situated externally to the nerve
cord.
(2) The cirrus pouch and the vulva are in one plane dorso-
ventrally.
(3) Jt differs from A . centripunctaia with regard to the position
of the uteri in that in southwelli they alternate from side
to side in the male mature as well as in the gravid
segments, whilst in A. centripunctaia they are practically
in one row in the male mature region as well as in the
gravid strobila.
I propose for this new species the name of Avitellina southuDelli,
in honour of my teacher, Dr. T. Southwell, and in recognition of
his unfailing help.
(7) Avitellina gegyptiaca, n.sp.
Host : — Cephalopus sp. (Duiker).
l^ocality : — Nagoa, N.E. Rhodesia, Africa.
The fragments examined measure from 2 cm. to 10 cm. in length,
and from i mm. to i-8 mm. in breadth. They show no signs of
external segmentation, even if suitabl}^ magnified, but the genitalia
are segment ally arranged. The segments are very short and the
genital pores are irregularly alternate.
Excretory System, In an immature portion of strobila, 10 cm.
in length and 1*7 mm. in breadth, the arrangement of the excretory
vessels is peculiar in that the small dorsal vessels are situated laterally
to the large ventral vessels, and in this particular the worm resembles
Hexastichorchis pintneri Blei, 1921. The dorsal vessel is not coiled ;
it lies a little nearer to the ventral vessel than to the margin of the
worm, and measures, in this region, about 36/^ in diameter. The
ventral vessels are regularly coiled and measure about 72^ in
diameter.
In a fragment of the male mature strobila measuring 5 cm. in
367
length and i-6 mm. in breadth, the ventral vessels have a diameter
of about 130//. In transverse sections the two vessels are situated
in the same plane, and in the middle line of the dorso-ventral diameter
of the strobila.
Muscular System. The longitudinal muscles are arranged in two
layers, the inner is strongly developed, and has a thickness of 22//.
The fibres are more or less evenly scattered in this layer, and are not
formed into separate bundles. The outer is a subcuticular layer
and is situated immediately below the cuticle, and is one fibre deep.
Male Genitalia. The testes are arranged in four rows, one
internal and the other external to the ventral excretory vessel,
and between the latter and the outer dorsal vessel on each side.
The outer row is two to three testes deep, the inner being four or
five, and very compact. Each testis is distinctly elongated and
measures about 90/^ by 54/^.
The vas deferens is thrown into several loose coils before it
enters the cirrus pouch. The latter is pyriform and measures
about 83/^ by 24^ ; it is always dorsal to the vulva on both sides,
and on the same plane dorso-ventrally. The genital ducts pass
dorsally to both the excretory vessels and the nerve.
Female Genitalia. The ovaries are situated close to the poral
side of the uteri, and are ventrally placed ; each measures about
54//. The ovarian eggs measure about 16// in diameter. The
vagina is dilated to form a receptaculum seminis midway between
the ventral excretory vessel and tlic ovary. It is oval in shape
and measures about 90// by 24//. The vulva measures about io8/^ by
ii^, and is not covered by glandular cells.
The paruterine organs, when fully developed, are practically
arranged in alternating rows, and occupy the middle third of the
breadth of the strobila. Each measures about 245// by lOO//, and
has a semi-lunar fibrous pad in front of it. In gravid segments
the testes and ovaries have atrophied and the ventral excretory vessels
are straight and not coiled.
This species differs from all the others within the genus Avitellina
in that the small dorsal excretory vessel lies externally to the ventral
vessel although they are in the same transverse plane, as seen in the
cross-sections. It agrees with Blei's species, Hexastichorchis pintneri,
in this respect. It differs from it, however, in having only four rows
of testes, one on each side of each ventral excretory vessel, the outer
fjeing situated between it and the dorsal vessel ; thus, there are no
testes externally to the dorsal vessel as there are in H. pintneri.
In the latter species there are six rows of testes in the anterior
part of the worm, one internally to the ventral vessel ; one between
it and the dorsal vessel, and one external to the dorsal vessel. It
differs from A. centripunctata, as above stated, in the presence of the
small dorsal vessel, lateral to the large ventral vessel ; it also differs
from it in the presence of the paruterine organs in two rows in the
middle field of the strobila and in the cirrus pouches being always
dorsal to the vulvae and in one plane with them dorso-ventrally.
EXPLANATION OF LETTERING
c. Cirrus.
c.c. == calcareous corpuscles.
c. p. — cirrus pouch.
d. e.v. — dorsal excretory vessel.
e. = eggs.
f. p. — fibrous pad.
g. a. = genital atrium.
i.f.p. " intersegmental fibrous pad.
i./.w. — inner longitudinal muscle.
intJ. ~ interuterine duct.
i.m. — longitudinal muscle layer.
«. nerve.
0, = ovary.
od, — oviduct.
0. 1.m, = outer longitudinal muscle.
p,o. = paruterine organ.
p.p. — paruterine pouch.
T.S. = rcceptaculum seminis.
t. — testes.
1, m. = transverse muscle.
ut, — uterus.
ut.d. ~ uterine duct.
V. ~ vagina.
v.d. ~ vas deferens.
v.c.v. ~ ventral excretory vessel.
v,s. ” vesicula seminalis.
m. — vulva.
37 °
Dorsal.
Fig. 3. Stilesia globipunciata. Cross-section showing migration ova. x 45.
Anterior.
Posterior.
Fig. 4. Stihsia glohipunciata. Showing fully-developed uteri and the relation of the vulva to
the cirrus pouch. The ovaries have completely atrophied, x 33.
Anterior.
Posterior.
Fig. 5. Stilesia gloMpunctata, Partly gravid segments showing the shape of the fibrous structures
in front of the paruterinc organs, also the persistent testes and the dorsal excretory vessels, x 33.
371
Anterior.
Posterior.
Fig. 6. Rtilcsi a qlohi punctata. Gravid segments show^lng mature pnruterinc pouches, displaced
parutcrlne organs, the opening between them, and the strongly-developed hhrfius pads, and the still
persistent dorsal excretory vessels. x 66.
I'lG. 8. Sttlcsia vl<)hi pjinciala . Showing
variable shape <il' migrating ova. x 400-
Fig. 7. Stt'h’iia plobipunctata. Showing the
vulva, cirrus pouch arid genital atrium surrounded
by hair-like processes. x 4<")o.
Anterior.
Posterior.
Fig. 9. StiUsia vittata. Male mature segments showing the po.sition of the calcareous corpuscles
and the genitalia. X 60.
37 *
Dorsal.
Ventral.
Fig. io. Stilcsia vitlata. Cross-section showing the relation of the cirrus pouches to the
vulvac and the passage of the genital ducts between the excretory vessels, x 90.
Anterior.
Posterior.
Fig. II. Stilcsia vittata. Gravid segments showing the complete course of the vas deferens —
ovaries and dorsal excretory vessels have completely atrophied, x 30.
Dorsal.
Ventral.
Fig. 12. Stilcsia hcpatica. Cross-section in a male mature segment showing the relation of the
genital ducts to the excretory vessels, x 30.
Anterior.
Posterior.
Fig. 13. Stilcsia hcpatica* Gravid segments showing the paruterine organs and pottdies and
the relations of the cirrus pouches to the vulvae. x 30.
57 ^
Dorsal.
Ventral.
Fig. 17. AvitcUifw ccrttripunctata. Cross-section in the gravid region, x 30.
Fig. 18. AvitcUina ccniripnnctata. Showing paruterinc organ and pouch and an intcrsegmcntal.
pad. X 125.
Anterior.
Posterior.
Fig. 19. Ai'ifcllitia sudanca. Showing male mature strobila, x 30.
AiUL^O^ dl
Fig. 25. AvhelUna soutkwelli, n.sp. Showing the gravid
strobila. x 2$.
Fig. 26. Avitellina ocgyptiaca, n.sp. Showing
the immature strobila. The testes arc begin-
ning to develop, x 30.
Dorsal.
Fig. 27. Avitellina cegyptiaca, n.sp. Cross-section in the immature region, x 48.
Fic. 28, Avitellina cegyptiaco^ n.sp. Showing the .male mature strobila. x 32.
Dorsal.
Avitellina (rgypticu u^ n.sp. Showing the cross-scctlon in the male mature strobila.
Fjg. 30. AvitclUfui agyptiaca^ n.sp. Showing partly gravid strobila. x 30.
Fio. 31. Avitellina asgyptiacay n.sp. Showing gravid strobila. x 48'.
378
REFERENCES
Blei, Rudolf (1921). Drci neuc Schafzcstodcn. Ccntrhl. f. Bakt.y Oris., 87 , 365.
Gough, L. H. (1911). A monograph of the tapeworms of the sub-family AvitclUninac^ being a
revision of the genus Stilesia and an account of the histology of AvitelUna centripunctata (Riv.).
Quart. Jl. Microscop. Sci., 56 , 317 .
Southwell, T. (1929), Notes on the Anatomy of Stilesia hepatica^ and on the genera of the sub-
family Thysamsominae (including AviteUininae). Ann. Trop. Med. & Parantol.y 23 , 47 .
S'liLEs, C. W., and Hassal, A. (1893). A revision of the adult cestodes of cattle, sheep and allied
animals. U.S. Dept. Agric. Bur. Anim. Ind. Bull.., 4 .
Woodland, W. N. F. (1927). On three new species of AvitelUna (Cestoda) from India and the Anglo-
Egyptian Sudan, with a fc description of the type species A. centripunctata (Rivolta), 1874.
Ann. Trap. Med. & Parasitol., 21 , 385.
(1928). On a new genus of AviteUininae tapeworms from ruminants in East Africa.
Parantol)sy<, 20 , 56.
Plate V
3^0
EXPLANATION OF PLATE V.
Stilesia glohipunctata. Photograph showing the heads of the
worms deeply* embedded in the mucosa of the small intestine of
sheep. X 2.
Jnuah. oj I'rop. McJ. c"- P(ii-asili>/., \ \>!. XXf! f
PLATE V
/,V U/S'. M. 1.101,11
C. Tinliipj, <X Co., Ltd., Imp.
ON A NEW SPECIES OF
PHYLLOBOTHRIUM (P. MICROSOMUM)
FROM AN INDIAN SHARK
BY
T. SOUTHWELL
AND
I. S. HILMY
{Received for publication 22 Jtdy, 1929)
Four specimens of this cestode have been obtained from tiie
intestine of Gingly mo stoma concolor. Pearl Banks, Ceylon. Pearson.
No. 158. 9.3-21.
The worms are very minute and measure from 2-2 mm. to 2-4 mm.
in length ; they are composed of six or seven segments, the last
one being nearly as long as the rest of the worm, and measuring
about I mm. in length. The maximum breadth of the worm varies
I'lG. I. Phyllobothrium microsomum. Entire worm, x 3S. _ Original.
3S*
382
from 234// to 312//. The genital pores are difficult to locate ; they
are irregularly alternate and situated a little behind the middle of the
lateral margin of the segment. The head consists of four unarmed,
boat-shaped bothridia borne on short stalks, each having a length
of about 350// and a breadth of 200 fjb. Their margins are definitely
thickened, the rim having a breadth of about 17/^; their shape
and appearance vary considerably. Accessory suckers are absent,
as is also a myzorhynchus. There is no neck.
Owing to lack of material nothing is known regarding the
excretory, muscular and nervous systems.
Fig. 2. rbyllohotbrium microsomum. Penultimate segment, x 192. c.p. — cirrus pouch 5
0. — ovary ; s.g, — shell gland ; t. — testes ; ut. — ^uterus j va, — vagina ; v.g , — vitelline glands. Original.
Testes, These first appear in the second or third segment and
reach their maximum development in the last ; their disposition in
the latter is very different from that in the other segments ; thus, in
the penultimate one they are arranged in capsules, these being
disposed in two longitudinal rows, one on each side of the median
383
axis. There are about twenty-five capsules on each side ; they
lie with their longer diameter transversely, and each measures
about SOju by i 6 fz. In the last segment the capsules have
disappeared entirely and the testes lie free, occupying the greater part
of the segment, the bi-lateral arrangement having been lost.
The writers wish to point out that this condition obtains in quite
a number of species of Tetraphyllidea but has hitherto not been
described.
The cirrus sac in the penultimate segment extends about a third
the distance across, its internal extremity being directed anteriorly.
The vas deferens is only slightly coiled and is situated close to the
medial extremity of the sac.
The ovary is U-shaped, each limb being bifid ; the aporal
limbs are slightly longer than the poral and extend along the lateral
margin almost to the middle of the segment.
The vagina is a simple thick-walled tube which, from the pore,
runs anteriorly to the cirrus sac. The vitelline glands consist of two
rows of acini, one running along, and close to, each lateral margin of
the segment.
The shell gland is prominent and situated in the concavity of the
ovary ; it measures 25// by 31//. Immediately anterior to it can be
seen the two oviducts, one from each ovarian limb, which meet in
the middle line. They are continuous with the vagina and the uterus.
Uterus. Only the rudiments of this organ could be seen and this
consisted of a granular condensation resembling a tube running along
the median longitudinal axis.
As in practically all other species of this family, gravid segments
and eggs are unknown. The species differs from others hitherto
described in size and in being composed, when fully matured, of
only about six proglottides.
On account of its small size it has been given the specific name of
microsomum.
BO THRIOCEPHAL US SCORPII
(Mueller, 1776) Cooper, 1917
BY
I. S. HILMY
Dr. med. (Berlin), D.T.M., D.T.H. (Liverpool)
{From the Parasitological Department, Liverpool School of Tropical
Medicine)
Received for publication 15 August, 1929
Synonymy extensive including the following : —
Vermis multimembris rhombi Leeuvenhoek, 1722.
Taenia scorpii Mueller, 1776.
Alyselminthus bipunctatus Zeder, 1800.
Taenia punctata Rudolphi, 1802.
Bothriocephalus punctatus Rudolphi, 1810.
The specimens to be described were obtained from the National
Museum of Wales, bottle 28, 25.7.9, dated May 6th, 1928, collected
from a turbot 3*5 miles south of Penkilan Head, Wales. They were
preserved in 5 per cent, formaldehyde. The longest incomplete
worm, still attached to the intestine, measured 26*5 cm. by 5 mm.,
and the smallest immature worm 1*25 cm. Many strobila with
their scoleces, both gravid and immature, were found free in the
bottle. They measured as follows : —
Smallest.
Largest.
(i) Immature fragments with scolex...
9'5 mm. by i>6 mm.
5*1 cm. by 21 mm.
(2) Immature fragments without scolex
1*9 cm. by i'6 mm.
5 cm. by 2*1 mm.
(3) With scolex and gravid segments
About 7*15 c
m. by 8*5 mm.
(4) Same without scolex
2*5 cm. by 7 4 mm.
6*7 cm. by 4*8 mm.
(5) Fragments consisting of gravid segments only ...
1-3 cm. by 4»2 mm.
14 cm. by 6 mm.
No mature segments either with or without scoleces were found
free in the bottle.
385
386
The colour of the preserved material is greyish-white. Crenulation
of the lateral margins is just visible to the naked eye.
The scolex measures from 1-56 to 2*75 mm. in length by 940/i to
1*09 mm. in breadth by about 780// in thickness. It is variable in
shape in the preserved material. Its greatest breadth is found
near the middle. The anterior extremity is sometimes as broad
as the posterior, but it may be either broader or narrower, and the
same applies to the thickness. The scolex terminates anteriorly
in a square disc the face of which is usually a little concave but it
may be convex. A slight to moderate constriction situated behind
the terminal disc is always present. At the posterior third of the
scolex there is often a transverse groove, not well marked. This is
believed to be the beginning of the strobila.
Fig. I. Bothriocephalus scorpii. Heads. A, B, C, and E — surficial view ; D — lateral view. X 8.
Original.
Each of the two shallow bothria occupies the whole length of
the scolex ; they are very variable in shape. Some are broadest
at their anterior extremity and assume the shape of a V or Y.
They are usually deepest at about one-eighth the length of the
scolex from the anterior extremity. From this point they gradually
become shallower posteriorly, until the cancavity has disappeared.
In some specimens the sinuous margins of the bothria were seen in
lateral view.
The strobila begins immediately behind the scolex. The first
segment measures about 428// in length by 624^1/ in breadth and
312 jii in depth and it overlaps the anterior border of the second
segment. In the latter careful examination shows a shallow furrow
situated near the middle of each lateral margin. These become
more marked in the third and fourth segments, giving each of them
the appearance of the so-called double-segment. The latter increase
gradually in length and breadth. At about 2 cm. from the anterior
38 ?
extremity each segment giving rise to the ' double-segment ’ again
shows indications of secondary shallow furrows. Whilst these
furrows become increasingly marked posteriorly, the ' double-
segment ’ divides into two segments each of which is likewise double,
the anterior overlapping the posterior one. This process appears
to be repeated several times, and takes place quickly until mature
' double-segments/ with 3, 4, 5, or even 6 sets of genital organs,
are seen.
The formation of the secondary and tertiary furrows is apparently
either delayed, or does not take place at all in the posterior one of
the ' double-segments,’ the anterior thus exercising a predominance
over the posterior segment.
The genital rudiments appear in whole mounts at about i*6 cm.
behind the head whilst mature segments occur at about 3*3 to 5 cm.
from the anterior extremity. They measure 624/^ in length by
3*8 mm. in breadth.
Dark patches occur on one surface posteriorly ; these represent
the uterine sac filled with eggs. They alternate irregularly from
one side of the mid-line to the other, and are situated near the
anterior margin of the segment, but they may occur in the mid-line.
On the opposite surface the genital pores can be made out in the
unstained condition with a hand lens, as very minute, dark spots
situated in a median, discontinuous groove.
The cuticula is 6/^ in thickness and is formed of two layers ;
the outer, which stains more deeply, is composed of stout, closely-set
pseudo-cilia ; the internal is homogenous. Immediately beneath the
latter is a very thin, sinuous, retractile membrane.
About Tjjn internally to the latter membrane there is a layer of
matrix cells arranged radially and irregularly at different levels
and having a thickness of about A considerable number of
them is also found in other parts of the cortex and in the medulla.
In some specimens calcareous corpuscles measuring up to 18// in
diameter occur in abundance in the parenchyma.
The muscular system is composed of longitudinal, transverse,
and dorso-ventral muscle fibres. The longitudinal fibres are
comparatively abundant and form two layers, one external and
one internal. The external layer is made up of a few bundles
situated just beneath the cuticula. It can only be detected under
388
high-power magnifications and special staining inethods. The
internal layer occupies most of the space between vitelline glands
and medulla and consists of large numbers of bundles which vary in
thickness, those nearer to the vitelline glands are considerably
stronger than those near the medulla. The transverse fibres are
usually feeble and are situated between the internal, longitudinal
muscles and the medulla, thus forming a sac which encloses the
latter.
These transverse fibres are found to be slightly stronger between
the * double-segments,' evidence that internal segmentation takes
place. The dorso-ventral muscles are found in the medulla only,
especially in the lateral fields occupied by the testes and enclosing
the latter.
There are two longitudinal nerves, one on each side of the median
axis. Each nerve has a diameter of about 35^ and is situated at
equal distances from both surfaces and at about, one-fifth the breadth
from the lateral margin. They appear in cross-sections as semi-
circular, transparent structures and are surrounded, especially
laterally, by few cells, some of which may be ganglion cells.
Dorsal
Fig. 2. Bothriocephalus scorpii. Cross-section, x 25. Original.
The excretory system shows great variations. In the youngest
immature segments six longitudinal vessels, situated in the medulla
can be seen, whilst in slightly older, mature and gravid segments
they are very difficult to find. It appears as if they break up very
early into branches of different dimensions which frequently com-
municate together by anastomoses. In one longitudinal, dorso-
ventral (sagittal) section and at about one-quarter the breadth
from the lateral margin, a longitudinal canal, measuring xOfA in
diameter and following a sinuous course, is seen in the medullary
parenchyma and is believed to be one of the main excretory vessels.
3^9
In immature segments the parenchyma is occupied by longitudinal
muscles and special distinctive cells from which the genital organs
develop. At first, a longitudinal, transversal field of genital cells
which develop very rapidly is formed. All genital organs with the
exception of the vitelline glands are derived from these cells.
Another mass of special cells, from which the vitelline glands develop,
appears later beneath the cuticula.
The first genital organs to develop are the testes. They are
situated in a single layer in the medullary parenchyma forming two
longitudinal fields, one on each side of the median axis. They are
continuous from segment to segment and do not extend in front of
or behind the ovary. Each field measures 870/^ in breadth in a
gravid segment, 3*6 mm. in breadth and is situated at equal distances
from both surfaces and at about 300 to 350// inwardly from the
lateral margin of the segment. One set of genital organs comprises
about 44 testes in each lateral field, but this number varies greatly.
Their shape is subspherical (38/i by 42/^ by 42//) to ovoid (63//
by 28^ by 28/^) ; in the latter case the longer axis is directed
transversely.
In gravid segments the testes shew all stages of development
including primary testicular cells, morula-like cells, some with
peripheral arrangements of the nuclei ; elongated chromatin bodies ;
unripe spermatozoa and lastly fully developed ones. A thick tunica
propria is present. The vasa efferentia are very difficult to make
out. They are very fine and have a structureless wall.
The cirrus pouch measures about 122*5^ by yo^i and is broadest
at about the junction of its middle and proximal third. It is ovoid
in shape and is directed ventrally and slightly anteriorly. At about
its distal fifth it is slightly bent towards that lateral half which
contains only the smaller part of the uterine duct. This is invariably
the case in mature and gravid segments. Its wall is thick and
muscular and is covered on both surfaces with myoblastic nuclei.
Few muscle fibres are arranged in an irregular manner inside the
pouch*
At the proximal end of the cirrus pouch, immediately behind
the opening of the vas deferens into it, and closely attached to its
wall is a comparatively small vesicula seminalis interna which has a
maximum diameter of about 10 a. It is pyriform in shape and has
390
its wider extremity situated proximally. Gradually it becomes
narrow distally and at a distance of about iSju from the proximal
extremity of the sac its lumen becomes of the same diameter as that
of the ductus ejaculatorius. The latter is much coiled in mature,
less so in gravid, segments. Its lumen measures from about 2 to
2*5/7. in diameter, and its wall is composed of two distinct layers, the
inner of which stains more deeply and is continuous with the cuticula
surrounding the very deep genital pore ; its inner surface is not
smooth but ragged and its outer wall is apparently muscular and does
not extend beyond the cirrus pouch but is continuous with the
wall of the latter.
From its proximal to its distal extremities the canal has the same
structure and it is evident, therefore, that cirrus and ductus ejacula-
torius are histologically not distinct.
The vas deferens is a mass of coils situated in the anterior part
of the segment and laterally to the median axis. It occupies in
gravid segments a space which measures 40// in length, 225/^ in
breadth, and about one half the thickness of the segment. In mature
segments its lumen is much narrower than in gravid ones. As the
lumen becomes distended with spermatozoa it gradually becomes
wider, the walls become attenuated and tlieir cells atrophy leaving
spare, oval shaped nuclei. The proximal parts of the vas deferens
may attain a diameter of from 30 to 40 fi. The distal parts are
narrower (9/7), their walls are relatively much thicker, their nuclei
more conspicuous and numerous. Before it enters the cirrus pouch
the vas deferens has a lumen of about 7/7 in diameter and is sur-
rounded by a large number of prostatic cells situated for the most
part anteriorly. There is no vesicula seminalis externa but in one of
the segments the walls of the vas deferens could not be made out and
the whole mass of spermatozoa appeared to be enclosed in a sac,
whilst preceding and succeeding segments were as described above.
The vaginal pore is situated immediately behind and slightly
laterally to the cirrus pouch.
The vagina begins as a very narrow duct, 2*5/7 in diameter,
proceeding towards the centre and just posteriorly to the cirrus pouch
for a distance of about 45/7. In the succeeding 30/7 of its length
the lumen becomes gradually wider until it measures about 10/7 in
diameter, then it suddenly becomes as narrow as before at a point
391
75 /^ from its distal extremity and remains so for the next 30//. It
then becomes wider again as it proceeds towards the ovary. When
it has traversed a total distance of about 150// in a dorso- ventral
direction, and in a sinuous manner it makes a sharp curve posteriorly
and then laterally for a distance of about to approach the oviduct
from a lateral point. From its distal to its proximal extremities
the internal wall of the vagina retains its cuticular structure, but,
unlike the cirrus, its inner surface is smooth. The outer wall is
muscular. All along its course except in its narrower parts, the
vagina is seen distended with spermatozoa.
Fig. 3. Bothriocephalus scorpii. Female genital organs viewed along the longitudinal axis of the
segment. X i8o. Original,
The ovary is an antero-posteriorly flattened organ situated along
the transverse axis and at the extreme posterior extremity of the
segment. It measures about 112^ in length, 350 to 450/^ in
breadth and 50 /li in thickness. Its lateral parts are slightly thicker
and curved towards the dorsal surface. The isthmus is broad and
deep but it may rarely be shallow. It is convex towards the ventral
surface. The fact that the isthmus is nearer to one surface (izoju)
than to the other is the only indication as to which is the ventral
and which the dorsal surface of the two. At ab^ut its middle and
protruding towards the centre the isthmus is prolonged into a mass
of cells which here attain their maximum dimension, and are without
nuclei. One or two of these cells are seen in the lumen of the oocapt.
This is funnel-shaped, measuring 33/^ in diameter and is covered with
well-developed circular muscle fibres. Its axis is directed posteriorly,
slightly laterally, and, in some cases, slightly dorsally ; its narrow
39 ^
extremity opens into the oviduct. The latter begins as a wide sac
into which the vagina opens as stated above, and which measures
by ^OfjL by 37^, including its very thick muscular walls. On the
dorsal aspect of this sac the oviduct, which has a lumen of 8^ in
diameter and a wall 3/4 in thickness, proceeds for a short distance
in a dorsal direction ; it then partly encircles the yolk reservoir.
Immediately after it has received the common yolk duct from the
latter it becomes continuous with the ootype. This is situated just
dorsally to the yolk reservoir, to the dorsal margin of which it runs
parallel, that is, laterally and slightly anteriorly. Its lumen measures
8/4 and its wall is surrounded by the voluminous shell gland for a
distance of 120/4.
The continuaJ:ion of the ootype is the uterus. It begins as a
very narrow duct which becomes gradually wider as it proceeds
distally. In mature segments it forms two sinuous, transverse
layers. In cross sections the uterus can be followed easily, whilst
in whole mounts it is viewed along its longitudinal axis and it is,
therefore, seen as small circular structures which may he mistaken
for unripe eggs. .
m
The first layer is situated posteriorly and extends from the
ootype laterally towards the ventral surface, thereby crossing the
ovarian lobe anteriorly. From here, in a mature segment 3-6 mm.
in breadth the uterus crosses the whole breadth of the ovary anteriorly
towards the other side of the median axis for a distance of 350 ju ; it
then bends sharply to form the anterior layer. Its lumen has now
a diameter of about 45^ ; after a slightly sinuous course it becomes
narrower during its last curve, and approaches the uterine sac. The
latter is situated near the ventral surface, very often laterally, but in
some cases in the median plane. It is globular at first becoming
conical as the segments mature, until in gravid ones it extends nearly
throughout the whole depth of the segment ; its longest axis is
directed dorsally and slightly laterally, and posteriorly. In mature
segments it measures 75 // in its greatest breadth and 112// in depth;
in gravid segments the axis of the cone measures 245// and the
ventrally situated base loo/u in length by 175/i in breadth.
The walls of the uterus, which are lined with epithelial cells,
become gradually attenuated and the ceils atrophy as the lumen
becomes wider in order to accommodate the developing eggs. In
mature segments the junction between the uterine duct and the
sac is obliterated by a large mass of cells, the nature of which is
believed by some helminthologists to be glandular so as to facilitate
the passage of the eggs to the exterior. As mentioned above the
uterine sac becomes wider as it develops ; the obliteration between
the uterine duct and the sac becomes less marked, disappearing
later, and in the meantime a slit-like opening appears between the
sac and the exterior.
The vitelline glands are the last to develop. They occupy two
lateral fields in the cortical parenchyma, and are occasionally
represented towards the mid line by a few follicles. In addition
to this, and more frequently, a few follicles are present in the
medullary parenchyma between the testes. This confirms the state-
ment by Matz that one follicle may be found in some cases near
the lateral border of the ovary. They are ovoid in shape and
measure about 35 fi by 30 /u by yofi. The vitelline ducts are quite
variable in diameter in different segments ; in some cases they are
wide and are often found distended with yolk cells ; in others they are
very narrow and are difficult to follow. I'hey tend to anastomose
dorsally and ventrally. From each surface two ducts, one on each
side of the middine, arise and run towards the medulla. Near the
transverse axis, each duct meets the other from the opposite surface.
From each of these dorso- ventral duct^ another arises, one of which
is short and wide and forms the vitelline reservoir, when this is
present ; the other opens into the first. The vitelline reservoir
ovd.
Ventral
Posterior
Fig. 5. Botbriocepbalus scorpii. Sagittal section. X 90. Ori^nal.
measures 40 fi by 60/1 by 50^ and is ovoid in shape ; it is situated
dorsally to the ovary, its longest axis being nearly parallel to the
transverse axis of the segment. One pole, which receives the yolk
cells, is directed posteriorly and dorsally. F rom the other the common
395
vitelline duct arises. This has a diameter of 9^ and is short. It
opens into the oviduct just before this becomes continuous with the
ootype. In specimens with very wide peripheral vitelline ducts no
viteUine reservoir is usually found, but instead, two wide central
ducts, forming a U with both hmbs nearly parallel to the trans-
verse axis, one being shorter than the other. The common vitelline
duct arises from the convexity.
The shell gland is a voluminous organ measuring go/^ by I20/^
by 90/^, situated posteriorly and dorsahy. It is best seen in sagittal
sections where it is found to encircle the ootype, there being a clear
space between the latter and the gland. Processes from the gland
cells cross this space thus placing the gland in communication with
the ootype.
The eggs in utero are ovoid in shape and measure 80^ by 45 by
6o//. They are dark grey in colour and contain what appears to be
a very small ovum, this being surrounded by a dense mass of yolk
cells, and the whole being enclosed in a transparent envelope. The
egg-shell has a thickness of i//, only. Under the oil-immersion lens
what is believed to be a very narrow operculum has been observed in
few cases at one pole. This evidence was supported by the fact
that when the eggs were pressed under a cover-.slip and thus ruptured
they almost invariably did so in a position which would normally
be occupied by an operculum. In some cases the operculum was seen
still hanging to the ruptured egg and it measured 23/^ in breadth.
The writer wishes to express his indebtedness to Dr. T. Southwell,
of the Liverpool School of Tropical Medicine, for his valuable advice
and help.
ABBREVIATIONS
c.p.
r=r cirrus pouch.
u.
— \iterus.
e.
- eggs.
u,d.
— uterine duct.
Im,
rr longitudinal muscles.
u.p.
— uterine pore.
0.
ovary.
u.s.
= uterine sac.
00c.
r= oocapt.
V.
— vagina.
oot.
= ootype.
v.d.
r-r vas deferens.
ovd.
oviduct.
v.g.
— vitelline gland.
= shell-gland.
vt.d.
— vitelline duct.
u
= testes.
vt.r.
— vitelline reservoir.
t.m.
s= transverse muscles.
REFERENCES
Beneden, P.-J. van (1850). Recherches sur la faunc littorale Belgique. Mem. de I* Acad. Roy., 25 *
Cooper, A. R. (1918). North American Pseudophyllidean cestodes from fishes. Illinois Biological
Monographs, 55 .
Loennberg, E. (1891). Anatomische Studien ueber skandinavische Cestoden. Koengl. Svenska
Veteiishaps — Akademiens Handlingar, 24 *
Meggitt, F. J. (1924). The cestodes of mammals. Jena.
Nybelin, O. (1922). Anatomisch-systematische Studien ueber Pscudophyllideen. Gocteborg.
JARDUGIA PARADOXA, A NEW GENUS
AND SPECIES OF CESTODE WITH SOME
NOTES ON THE FAMILIES ACOLEID^
AND DIPLOPOSTHID^
BY
T. SOUTHWELL
AND
I. S. HILMY
(From the Parasitological Department, Liverpool School of Tropical
Medicine)
(Received for publication, 3 September, 1929)
Southwell, in 1926, gave a short description of a worm which, he
pointed out, was of doubtful systematic position, but which, in
certain anatomical features, resembled Diploposthe Igevis. His
account was as follows : —
‘ One specimen from a small heron (Ardca Azare, N.P, Nigeria, 20.viii.25.
Collected and presented hy Dr. LI. Lloyd.
'Lhc specimen was peculiar in that in tlic anterior lialf of the sirobila only a
single set of male genital organs were present and these were unilateral. About the
middle of the length of the worm the second set of male genitalia appeared suddenly^
but irregularly. Posteriorly a double set of male genitalia was present in all segment s
except in four, which bore a single set.
The female genital organs appeared about the middle of the length of the worm :
they were normal, except that in a few of the most posterior segments portions of the
ovary had not atrophied and they were a conspicuous feature of segments in which
otherwise only the cirrus pouches and uterus were visible.’
A full description of this unique parasite, which is now considered
as the type-species of a new genus, is given below : —
The length of the worm is approximately 8-5 cm. and the greatest
breadth 2*35 mm. For the purpose of examination it was cut into
four fragments.
The scolex measures 333/i in breadth. It is pear-shaped and
is provided with four unarmed, cup-shaped suckers, each of which
has a diameter of 130/^. The invaginated rostellum, which is pointed
at its anterior extremity, measures 244/t by 88//, and is armed with a
397
398
single crown of about ten hooks, each of which measures from
13 to i 8 jbi in length.
The first signs of segmentation are visible about Soo/x from the
anterior extremity. Here the breadth of the worm is i*6 mm.
The cuticula measures 2fxin thickness. It is composed of three
distinct layers, the external and internal of which are membraneous
and stain deeper than the intermediate, homogenous and com-
paratively thicker layer. The matrix cells are situated immediately
beneath the cuticula and have a thickness of about i5/i. The cells
are spindle-shaped with small, round nuclei.
Fig. I. yardugia paradoxa. Head, x 116.
There are three layers of longitudinal muscles. The external
layer is situated between the cuticula and the matrix, and is composed
of single bundles in diameter and placed at distances of about yji
from each other. The intermediate layer lies about 40/* from the
cuticula inwards, and is composed of groups of stouter bundles ; each
group measures about 15/^ in thickness, and occurs at distances of
from 15 to 40/^ from one another. The internal longitudinal layer
is the most strongly developed. It is situated about inwards
from the cuticula. The single bundles may attain a thickness
of 15/^ and are arranged in groups which may measure 35/i 01 more
in thickness.
There are two longitudinal sinuous excretory vessels in each
lateral half. The larger vessel is situated internally to the smaller
and at the junction of the lateral and middle quarters of the segment.
It measures from 50 to jOfi in diameter and lies at a distance of
399
about 140^ from the ventral surface, where the thickness of the
segment is about 420/^. The smaller vessel, which measures 4// only
in diameter, is situated at about laterally and 24^^ dorsally to the
ventral vessel.
Calcareous corpuscles are abundant and are found mainly in the
peripheral parts of the parenchyma ; they attain a maximum
diameter of about 12//.
The most striking feature of this worm is the arrangement of
the genital organs. In the first fragment, which measures 1*75 cm.
in length, the genital rudiments appear, in whole mounts, at about
1-6 mm. from the anterior extremity, and are at first situated in the
mid-line, but soon become confined to one lateral half, viz., the right
Fig. 2. Jardugia paradoxa. Eight segments with mature male genitalia. Dorsal view, x 26.
half. At 4*5 mm. from the anterior extremity these rudiments
become distinctly elongated transversely, the elongations forming
the male genital ducts, whilst the testes differentiate from the medial
parts. In about the 130th segment, which is situated i-6 cm. from
the anterior extremity, these genital structures become bilateral
owing to the striking and sudden appearance of male organs in the
400
left half of the worm where, previously, no rudiments have been
visible, the only difference being that two testes only are found in
this half against three in the opposite half. The succeeding segment
(the 131st) possessed one set only ; the second segment (the 132nd)
had double sets and the remaining few segments (the 133rd to the
142nd) had again each one set.
In the second fragment, which measures 3 cm. by 2-3 mm., the
male genital organs have attained their maximum development. The
first nineteen segments possess one set of male genital organs in the
right half. Then there were : —
Two male sets in the 20th ;
One male set in the 21st to 26th ;
Two male sets in the 27th, and
One male set in the 28th and 29th.
From the 30th to the 89th segment (the last in the second fragment)
the male genitalia were double, as was observed in the remaining
two fragments of the worm.
The testes are globular in shape and measure from 40 /i when
they first appear, to 123/x in mature segments. They are situated
in front of the ovary, in the anterior half of the segment and near
the dorsal surface ; they lie parallel to the transverse axis of the
segment and laterally to the median axis. In segments possessing
only one set of genital organs, there are usually three testes confined
to the corresponding half (the right half) ; two segments, however,
possessed two testes only. In the other segments with double male
genitalia, there are usually three testes in the right half and two
in the left half, but the number on each side varies between none and
four. Altogether there are from two to six testes in each segment.
They so6n begin to atrophy and sometimes disappear before the
female genital organs have attained maturity.
The vas deferens is short and inconspicuous. It arises anteriorly
to the testes and proceeds towards the lateral margin ; it very
rapidly widens into a vesicula seminalis externa. This conspicuous
organ, which is oval (seldom globular) in shape, is situated in line
with the cirrus pouch and at its proximal extremity ; it is very
variable in size, the largest measuring 2 yyfi by 140/i. It is generally
found distended with spermatozoa. Its lateral (distal) termination
extends beyond the proximal extremity of the pouch and remains
401
dorsally to the latter for a short distance ; it then narrows suddenly
and, turning in the medial direction for a short distance, eventually
forms a loop before it enters into the pouch. The latter organ is an
almost cylindrical sac with its longitudinal axis directed transversely ;
it measures from 380 to 625//- by 70 to 85//, and is situated in the
anterior half of the segment and near the dorsal surface ; it is either
straight, curved or sinuous, but in each case its distal extremity
is nearly always directed slightly posteriorly ; its proximal extremity
is at about the same position as the excretory vessels which the
pouch passes dorsally.
Just after the male genital duct enters into the pouch it widens
again into an internal vesicula seminalis. This is elongated and
measures up to 210 /a ; it is often as broad as the pouch itself, being
broadest at its distal extremity, where it narrows suddenly and
becomes continuous with the ductus ejaculatorius. The latter is an
almost straight duct when the cirrus is protruded ; it measures
175// by 10// ; its proximal extremity has a wide lumen (17//) and is
provided with a strong sphincter muscle.
The cirrus, which in mature segments nearly always protrudes
about 85//, measures 210// in length. Its protruded part is covered
with fine, closely-set spines, each of which measures about 3//, and
which have a linear arrangement. The junction of cirrus and ductus
ejaculatorius, within the cirrus pouch, is surrounded by a dense mass
of prostatic cells.
The genital sinus, which has a diameter of 70//, rarely lOO//, and
a breadth of 52//, is situated at about the junction of the anterior
and middle thirds of the lateral margin of the segment.
The vagina lies ventrally to the cirrus pouch ; it begins with a
diameter of 24// and, as it proceeds inwardly and parallel to the
cirrus pouch, its lumen narrows gradually over a length of loo// until
it has a diameter of 7//. Its diameter then varies between 7// and 15//
until it has passed, together with the cirrus pouch, dorsally to the
longitudinal excretory vessels. When it has thus covered a total
distance of 625// or, at the junction of the lateral and middle quarters
of the segment, it turns suddenly and, for a very short distance,
dorsally ; later, with a distinctly wider lumen but of variable size,
it follows a sinuous course posteriorly and medially towards the ovary,
thus passing posteriorly and eventually ventrally to the testes. At
402
its proximal (central) extremity the lumen becomes distinctly wider
and an oval to pyriform receptaculum seminis is formed which may
measure up to 6o^ by 90//.
As in the male, so in the female, the duplication is at first
irregular ; thus in the second fragment, above-mentioned, segments
Nos. I to 25, 27 to 49, 52 to 54, 58 to 65 and, lastly, 67, possess only
one set of female organs with the exception of the vagina which,
where double male genitalia occur, is also doubled, in which case it
always communicates with the vagina of the right half, thus forming
a transverse arch across, and dorsally to, the female organs. In
these cases also, there may be one receptaculum seminis or two, but,
more frequently, this organ is absent.
▼.d. T. 9.1. pr.
u. ▼.
ViG. y,. Jardugia paradoxa. Segment with mature female genitalia. 'Fhe testes are almost
atiophicd. Dorsal view. X 36.
It should be noted, firstly, that in segment No. 19 (of the second
fragment) which, as mentioned above, possesses two sets of male
and one set of female genital organs, the left vagina extended only
to the point where it usually, when mature, changes its transverse
course into a posterior and medial one to approach the ovary ;
secondly, in segment No. 50, which, as mentioned above, possesses
two sets of both male and female organs, the same was observed with
the left vagina, the unusually wide proximal end of which apparently
ends blindly and has a diameter of 44/^.
The ovary appears at about 9*6 mm. as a small collection of
cells situated posteriorly to the testes and near the median axis.
This mass of cells soon increases in size and elongates transversely ;
it then becomes slightly curved antero-posteriorly, the concavity
being directed posteriorly. The ov€uy continues to increase in
size in the posterior segments until it occupies the middle third of
the breadth and more than three-quarters of the length of the
segment. Here the single ovarian follicles are globular and have a
diameter of yojj,. They are very numerous and are arranged irregu-
larly around the female ducts, the concavity being directed dorsally
and posteriorly. Several attempts to determine the exact number
of follicles present in each ovary failed, but they may number at
least forty. In their last stage of development the ovaries cease to
function and, later, disappear suddenly and irregularly, so that in
some segments they are absent altogether whilst preceding and
succeeding ones contain only traces of the organ.
The vitelline gland is the most posteriorly situated of all organs
and is nearer to the dorsal surface than to the ventral. It is deeply
lobed and occupies up to 70// of the length and 160// of the breadth
of the segment. It discharges the yolk cells into the oviduct from
a posterior and eventually dorsal point.
The oviduct is short and wide and arises from the dorsal aspect
of the ovary ; after receiving the yolk duct it becomes continuous
with the ootype. This is very short and sinuous and is directed
anteriorly to open, after passing through the inconspicuous shell
gland, into the uterus. The ootype from each side may open
separately into the uterus or each may proceed anteriorly and
medially to meet the ootype of the opposite half, thus forming an
arch from the convexity (anterior aspect) of which the uterus proceeds
anteriorly for a very short distance (about 85/^).
The uterus is seen at first as a transverse line of cells penetrating
in its middle parts between the ovarian follicles. It may extend,
whilst still in this stage of development, beyond the longitudinal
excretory vessels, which it crosses dorsally. When mature it
becomes very wide and increases so much in length that it becomes
sinuous to accommodate itself in the limited and even decreased
breadth of the segment. No fully gravid segments were found
and accordingly the eggs are unknown.
The new genus Jardugia is defined as follows : —
Scolex with an armed rostellum. Each segment of the strobila
has a single or double set of male, situated in front of a single or
double set of female genital organs. Uterus a transverse sinuous sac.
Adults parasitic in birds.
Type-species : — Jardugia paradoxa n.sp.
40 +
Up to the present the following species of cestoda have been
recorded from Ardea : —
Ardea cinerea Linn.
Dilepis campylancristrota (Wedl, 1855).
Acanthocirrus cheilancristrota (Wedl, 1855).
Hymenolepis microcephala (Rndolphi, 1819).
Tsenia leuckarti Krabbe, 1869.
Ardea spp.
Tasnia leuckarti Krabbe, 1869.
Anomotasnia aurita (Rudolphi, 1819).
Dilepis hoplites (v. Linstow, 1903).
Systematic. The family Dilepidid^ Railliet and Henry, 1909,
is divided into the following three sub-families : —
(1) Dilepinin^. Uterus persistent.
(2) Dipylidinje. Uterus replaced by egg capsules.
(3) Paruterinin^. Uterus developes paruterine organs.
It is clear that, as the uterus in our species is persistent, the
only sub-family to which it might be referred is Dilepinin^:. But
none of the genera in this sub-family is characterised by the possession
of a double set of genital organs.
The characters of the family AcoLEiDiE Ransom, 1909, are as
follows : —
‘ Tajnioidea : Scolex generally armed, seldom without rostcllum. Suckers
unarmed. Strobila thick with short segments. Musculature consists of at least
two layers of longitudinal muscles alternating with layers of transverse muscles.
A single set, double set, or partial duplication of reproductive organs in each segment.
Male genital openings marginal. Female genital (vaginal) opening lacking. Cirrus
always very large and armed with strong hooks or spines. Eggs with thin transparent
shells. Adults in birds.’
Type-genus : — Acoleus Fuhrmann, 1899.
It contains the following genera : — Acoleus Fuhrmann, 1899,
Diploposthe Jacobi, 1896, Gyroccelia Fuhrmann, 1899, Dioicocestus
Fuhrmann, 1900, Diplophallus Fuhrmann, 1900, Shipley a Fuhrmann,
1907, Progynotasnia Fuhrmann, 1909, Proterogynotxnia Fuhrmann,
1911, Urocystidium Beddard, 1912 and Monoecocestus Beddard, 1914,
in all of which a vaginal pore is absent except in the genus Diploposthe.
Fuhrmann, in 1926, placed the genus Diploposthe in the family
Hymenolepidid^ on account of the fact that there are usually
three, rarely seven, testes in each segment.
Poche, in the same year, created a new family Diploposthid^b, to
accommodate the genus Diploposthe which clearly could not be
405
retained in the family Acoleid^. He defined the family as
follows : —
‘ Taeniinca with flattened bodies, distinct internal and external segmentation,
a rostellum with one crown of hooks, unarmed suckers, short proglottides which have
no appendages. The musculature, from the exterior to the interior consisting
of a weak diagonal muscle layer, a strong, circular muscle just in front of the posterior
margin of the proglottis, a complete external and an incomplete internal layer of
longitudinal muscles and a layer of transverse muscles. Double genital pores each
situated at the lateral margin in a genital sinus ; centrally situated genital glands of
which the female are in front of the male ; three to (?) seven testes ; a vesicula
seminalis, a strongly developed cirrus pouch and a cirrus armed with strong spines
in each lateral half ; a bilobed ovary in front of the vitelline gland ; a simple, sinuous,
transverse uterus which forms several huge diverticula ; vagina double and opening
ventrally to the cirrus ; eggs, when ripe, have, in addition to the very thin, extensible
and transparent egg-shell, two more thin coverings.’
Of the ten genera referred to in the family Acoleid^, three,
viz., Diploposthe, Diplophallus and Dioicocestus , differ so widely
from the rest that it appears desirable to separate them.
Southwell, in ' The Cestode Fauna of British India ’ (in the press)
places the genus Dioicocestusi in a new family which he names
DioicocESTiDa2, the character of which is that the sexes are separate.
In the genera Diploposthe, Diplophallus and Jardugia n., the
genital organs show either complete or partial duplication. The
following table will emphasize the relationship between them : —
Diphposibc
Diplophallus
yardu^ia
Male organs
Double in each segment
Double in each segment
Singhs or double in
each segment
Number of testes in
each segment
3 to 7
About loo
3 to 5
Position of testes
Posterior to ovary
In two lateral fields
Anterior to ovary
Female organs
Single in each segment
but with two vagina
Single in each segment
but with two vaginae
■
Single or double with
1 one or two vaginae
Vaginal pore
Present
Absent
1
Present
Uterus
1 A transverse, sinuous sac
A transverse, sinuous sac
A transverse, sinuous
sac
It will be seen that these three genera form such a natural group
that, as they differ so widely from the remaining genera of the
family Acoleid^, the writers propose placing them in the family
DiploposthiDuE Poche, 1926, the definition of which is accordingly
emended as follows : —
Head with an armed rostellum. Mature segments broader than
long. Musculature well developed. A single or double set, or a
partial duplication of male and female genital organs in each segment.
Vaginal pore present or absent. Cirrus very large and armed with
spines. Uterus a transverse, sinuous sac. Adults parasitic in birds.
Type-genus : — Diploposthe Jacobi, 1896.
It now becomes necessary to re-define the family Acoleid^
Ransom, 1909, which is accordingly done as follows : —
Scolex usually armed. Musculature consists of at least two
layers of longitudinal alternating with layers of transverse muscles,
except in the genus Monoecocestus. A single set of genital organs
in each segment. Vaginal pore absent. Adults parasitic in birds
and mammals.
Type-genus : — A coleus Fuhrmann, 1899.
EXPLANATION OF LETTERING.
c. ^ cirrufi.
c. p. = cirrus pouch.
d. e.v. = dorsal excretory vessel.
d.ej. = ductus ejaculatorius.
0. = ovary.
pr. — prostatic cells.
r.s. «= receptaculum seminis.
sb.g. = shell gland.
t. = testes,
w. = uterus.
V. ~ vagina.
v.d. = vas deferens.
v.e.v. = ventral excretory vessel.
v.s,c. vesicula seminalis externa.
v.s.i, — vesicula seminalis interna.
vug. — vitelline gland.
REFERENCES
Fuhrmakn, O. (1908). Die Cestoden der Vogel. Zool. yabrb., Suppletnentband 10, 140.
(1926). Catalogue des invcrtebris de la Suisse. Fascicule 17. ‘ Cestodes.
Johnston, T. H. (1912). On a re-examination of the types of KrcffPs species of cestoda in the
Australian Museum, Sydney. Records of the Australian Museum^ 9, 4-13.
PocHi, F. (1926). Das System der Platodaria. Arcb,f. Naturg.., Abt. A., 91, 383-384.
SouTHyntLL, T. (1926). Cestodes in the collection of the Liverpool School of Tropical Medicine.
Ann. T rop. Med. ^ Parasitol., 20, 225-227.
WolffhOgel, K. (1900). Beitrag zur Kenntnis der VogelhelmintJs^ Dissertation, Universit. Basei
Freiburg i. Br.
DESCRIPTIONS OF THE EARLY STAGES
OF TWO FURTHER MOSQUITOS
COLLECTED IN SOUTHERN NIGERIA
BY MR. L. H. DUNN
BY
A. M. EVANS
{Received for publication 14 October, 1929)
In a previous paper I described the larva and pupa of Aedes
{Armigeres) albomarginata var. dunni taken by Mr. L. H. Dunn,
in Lagos, when a member of the West African Yellow Fever Com-
mission in 1927. The two larvae and pupae which form the subject
of this paper were also collected and reared to the adult stage, in
and near Lagos, by Mr. Dunn, to whom I am greatly indebted for
the privilege of describing them.
HARPAGOMYIA FARQUHARSONI Edw.
The larva and pupa of this myrmecophilous species have many
features in common with those of H, genurostris {splendens) described
by de Meijere (1911), and H. trichorostris , recently described by
Ingram and Meillon (1927).
Larva (fig. i, A-D). 'I'he shape of the head resembles that of
H. genurostris and H. trichorostris, being rounded in front and
widest along the posterior border. The clypeal hairs {cl.) are
multiple tufts of subplumose branches and project well beyond
the anterior border of the head. The inner anterior are composed
of 7 to 8 branches ; outer anterior 5 to 7 ; posterior 2 or 3. The
dorsal hair rising in front of the base of the anterior is 7 to 9 branched.
Frontal hairs are not present in the normal position but, internal to
the eye are two very delicate, branched hairs. From the lateral
margin a small branched hair projects and ventro-laterally are
three tufts, the anterior of about 10, the mid 4 and the posterior 6
branches. Small palmate tufts of 4 stout bristles lie posteriorly
on the ventral surface. The antennae are small, slightly curved and
407
4o8
narrowing distally with a double hair on the distal half. Mental
plate, as in H. tr ichor ostris, very narrow from before backwards,
with 12 teeth (ii well developed), on each side of the central tooth.
Fig. 1 . Harpagomyia farquharsoni Edw. A.'-D . — Fourth stage larva. A. — Head, dorsal
aspect and anterior edge of pro thorax (feathering of hairs not showiv) ; B . — Terminal segments of
larva, lateral aspect ; C . — Spines of lateral comb ; D . — Spines of pecten j E . — Pupal trumpet.
A and B to same scale, C and D to same scale, cl . — Clypeal hairs.
Thorax. As in H. trichorostris, the prothorax bears dorso-
laterally conspiciuous, fan-like tufts of many feathered hairs arising
from chitinous tubercles. There are a long and a short tuft on
each side in this species and a group of 3 long bristles completes
the anterior dorsodateral series ; the ventro-laterals are a single and
a triple bristle and a shorter tuft. The hairs of the anterior border
are shown in fig. i, A. The meso- and inetathorax bear fan-like
tufts of hairs dorso-laterally, which are much less conspicuous than
those of the prothorax. The dorso-lateral series of the meso-
thorax is completed by two long, simple, and one double bristle,
and a much shorter, fan-shaped tuft. The ventro-laterals are a long
fan-shaped tuft and a single bristle. The meso thorax also possesses
a dorsal row of 4 simple and a bifid hair at each side. The dorso-
lateral series of the metathorax are a long and a short fan-shaped
tuft and there is a well-developed tuft ventro-laterally. Dorsally,
at each side, is a group of 4 short multiple hairs. There is no palmate
bristle on this segment as in H. trichorostris.
Abdomen, On the first and second segments the dorso-lateral
plume is composed of 6 to 8 long, forwardly-projecting, bent, plumose
hairs and below them a 2- or 3-branched, shorter, stout, bent hair.
On the first segment shorter tufts are arranged as follows : dorsally
a quadruple tuft near the posterior border ; dorso-laterally a tuft
and a simple and a bifid hair above the base of the plumes ; laterally,
in front of the plumes, a longer fan-like tuft of about 9 straight
hairs ; ventro-laterally a tuft of 5 to 7 delicate hairs below the plumes,
and more anteriorly and medially a tuft of 2 to 5 longer and rather
stouter hairs. There is also a minute yentro-lateral tuft near the
posterior border. The second segment only differs from the first
in the possession of an additional minute, ventro-latcral tuft, and
the absence of the anterior, ventro-lateral large tuft. On the
remaining segments the dorso-lateral plumes consist of long, straight
bristles, multiple (2 to 4), on the third to fifth segments, and single
on the sixth and seventh. The dorsal and dorso-lateral tufts are
similar in the last five segments to those of the first, but the posterior
dorso-lateral tuft increases in size as far as the sixth segment ; on the
seventh it appears to be absent, the dorsal tuft having become
lateral in position. The large ventro-lateral series of tufts is well-
developed and increases in size on the posterior segments, that of the
seventh being longer than the segment. The ventro-lateral series
of minute tufts and hairs increases in number posteriorly. The lateral
comb consists of about 28 teeth and a few very small ones, arranged
in a sub-triangular patch, longer teeth as in fig. i, C. The group
of hairs and tufts beyond the comb is slightly variable, usually as
shown in fig. i, B. The siphon is rather weakly chitinised, the
length about three and a half times basal width ; it bears dorsally,
two rows of 5 tufts, usually as in fig. i, B, but variable and some-
times asymmetrical. Ventrally there is a single row of about
6 simple or 2- or 3-branched hairs ; on the basal third each side
bears a prominent tuft of 3 to 4 feathered hairs. The pecten is
very variable in the number, arrangement and shape of the teeth.
There is usually a basal patch of fringed teeth, which are sometimes
short and broad, and an irregular row of elongated, fringed teeth
extending along the basal two-thirds of the siphon, as in fig. i, B.
The tergite of the tenth or anal segment bears well-developed spines
distally, as in H. trichorostris. The clinging (dorso-apical) bristles
are usually a tuft of seven and a single very long bristle at each side.
The ventral fin is represented by a pair of long double or triple
hairs ; a plume of 6 hairs arises laterally from the distal edge of the
tenth segment. The anal gills are very long and wide, more than
twice the length of the last segment.
I'his larva differs from that of H. trichorostris and H, genurostris
chiefly in the large number of branches composing the clypeal and
other head tufts. From the former it also differs in not possessing
palmate tufts of short bristles on the metathorax. The great
variability of the pecten spines is a noticeable feature.
Pupa. This is essentially similar to those of //. trichorostris
and H. genurostris, possessing the peculiar triangular paddles which
are fringeless and without any apical bristles, the fan-like tufts at the
postero-lateral angles of the seventh and eighth abdominal segments
and the long double post-ocular bristle. As in H. trichorostris the
dentritic bristles on the first abdominal segment are rather poorly
developed and the sublateral bristles are very long on segments
five and six.
The cephalothorax is sub-pyriform in shape. The respiratory
trumpet is rather short and stumpy, the length is about two and a half
times the greatest width. When the pupa is mounted laterally,
the trumpets appear widest in the middle (fig. i, E). The opening
is almost at right-angles to the long axis ; seen from above it is
about twice as long as wide and appears constricted at about the
4II
middle. In addition to the long, double, post-ocular bristle is a short
double, inferior one. The antero-thoracic are a single, two bifid and
a trifid hair ; the dorsal hair is simple and external to it is a triple
hair (? supra-alar). As in H, trichorostris the mid postero-thoracic
hair is simple and the outer double, but the internal may be either
single or double. The longer bristles on the abdominal tergites are
as in H, trichorostris, but there are also a number of small, associated,
single and double hairs not referred to in the description of that
species. Of these there are 3 on the second, fourth and fifth segments,
2 on the seventh and i on the third and sixth. The paddles have the
mid-rib indistinct.
The long, double post-ocular bristle ; small, triangular, fringeless
paddles and the fan-like tufts on the seventh and eighth segments
are characters supporting the view put forward by Edwards (1922),
that the genus Harpagomyia should be included in the Sahethine
group.
Female. In one mature pupa the spermathecae are well
shown. They are almost globular in shape, the median much larger
than the other two, its diameter being at least one and a half times
that of either. The specimens did not show a scaled area between
the eyes.
Described from several larvae and pupae well preserved in spirit,
taken in leaf-whorls of the pineapple plant, near Yaba, Southern
Nigeria, 1927, Mr. L. H. Dunn.
The identification of the adults was kindly confirmed by Mr. F. W.
Edwards.
Mr. Dunn states that he found the mosquito breeding in
abundance in the central leaf-whorls of the pineapple plants in the
bush near Yaba. He suggests that the fan-like tufts on the pro-
thorax ‘ may signify that the larvae are able to move about in the
leaf sheaths in order to remain in the water.'
CULEX {CULICIOMYA) CINERELLUS Edw.
It is probable that the larva illustrated by Wesche (1910) and
described as ' Pectinopalpus fuscus Theo. ? (i) 'is that of C. cinerellus.
As, however, there are certain differences between Wesche's larva
and those from which Mr. Dunn has bred adults of C. cinerellus, the
latter are briefly described below. No description of the pupa
appears to have been published.
Larva (fig. 2, C). This larva closely resembles that of C. macfiei
Edw. (Macfie and Ingram, 1923), in the characters of the head and
the shape of the siphon tube. The siphon measures about i*2 mm.
' 0'5tniuitn«r€
Fig. 2. Culex {Culiciomyid) cinerellus. A . — Abdomen of pupa, dorsal aspect, except
first segment (very minute hairs not shown) ; B . — Pupal trumpet ; C . — Terminal segments of fourth
stage larva, spines of lateral comb and pecten shown enlarged as indicated ^ 1 . — Lateral bristle
(Seta A) ; sm . — Submedian bristle (Seta C).
Head. The chaetotaxy and antennae are as in C. macfiei : the
mental plate with lo or ii teeth on each side of the central tooth.
Thorax. The bristles of the anterior border are long ; and lateral
plumose tufts developed.
413
Abdomen. Lateral tufts are present on the first two segments.
The lateral comb (fig. 2, C) consists of about 40 fringed spines, the
posterior ones rather broad distally. Subsiphonal tuft of about
4 plumose hairs. The siphon is long and slender, the length about
eight times the basal diameter ; it is rather weakly chitinised. Two
small double hairs and a distal simple hair lie on each side of the
siphon ; the arrangement of the proximal setae is variable. The
pecten consists of about 12 spines which show, in a certain position,
long bifid ends ; each has a large tooth arising from the base and a
very small basal tooth is frequently present. The tenth segment is
lightly chitinised, and the ventral fin not well developed. The gills
in the specimens are very long and thin, but the shape may have been
altered in the process of moulting. They appear to be all of nearly
equal length.
Pupa. The pupal pelt is small and lightly chitinised. The
respiratory trumpet (fig. 2, B) is brown, darker on the basal half,
and relatively narrow with a small opening. Tn one position the
distal half is slightly wider than as shown in the illustration.
Abdomen (fig. 2, A). The paddles resemble those of C. macfiei
in shape, but the terminal setae are very minute. The dorsal
abdominal chaetotaxy differs considerably from that of C. macfiei,
in the numbers of the branches of most of the tufts. In C. cinerellus
the submedian (‘ Seta C,’ Macfie, 1919), on segment three, has from
3 to 5 branches ; that of the corresponding segment in C. macfiei
being composed of 15 to 17 branches ; on segments five, six and seven,
these bristles are single in the latter species, but are triple in
C. cinerellus. The laterals ‘ Seta A ' on segments two to six are
double in this species, but single in C. macfiei.
Described from several larval and pupal pelts of the specimens
taken in crab-holes, Lagos, 1926, Mr. L. H. Dunn.
Mr. Dunn stated that he found this species breeding in abundance
in many of the crab-holes in Lagos.
REFERENCES
Edwards, F. W. (1922). A revision of the genus Harpagomyia. Trans. Ent. Soc. Land., 1921, p. 496.
Ingram, A., and De Meillon, B. (1927). A mosquito survey of certain parts of South Africa, with
special reference to carriers of malaria and their control. Part 1 . Publications of S. Af. Inst,
for Med. Res., No. 22, 4 , 1-81.
Macfie, J. W. S. (iqiq)* The chaetotaxy of the pupa of Stegomyia fasciata. Bull. Ent. Res., 10 , 161.
Macfie, J. W. S., and Ingram, A. (1923). The early stages of West African mosquitoes. Part IV.
Bull. Ent. Res.y 13 , 409.
De Meijere, j. C. H. (1911)* Zur Metamorphose der Myrmecophilen Gulicide Harpagomyia
splendent de Meij. Tijds. voor Ent., 54 , 162.
Ws9Ch£, W. (1910). On the larval and pupal stages of West African Culicidae. Bull. Ent. Res. , 1 , 7,
NOTES ON CERTAIN VARIETIES OF
ANOPHELES MARSHALLI Theobald
BY
A. M. EVANS
{Received for publication, 14 October, 1929)
During the course of his recent survey of the mosquitos of the
Stanleyville Region of the Belgian Congo, Dr. J. Schwetz has bred
out a number of specimens of A. marshalli var. moucheti, and a
specimen which is evidently var. hargreavesi. From material which
he has very kindly sent to me, I am able to describe the larva and
pupa of the former and the pupa of the latter. As there are con-
siderable differences between the pupa of A . marshalli var.
freetownensis and both of those discovered by Dr. Schwetz, that of
the Freetown variety is described as well. With the help of
Dr. Schwetz's material it has been possible to examine the male
terminalia of a series of var. moucheti and, as a constant distinction
exists between that variety and var. freetownensis in these structures,
I have also included a brief description of them and illustrated the
chief points of difference.
ANOPHELES MARSHALLI var. MOUCHETI Evans
The larva and pupa of this variety differ rather markedly from
those of A. marshalli var. freetownensis, and also from the larva of
A . marshalli described by de Meillon, as well as from that of marshalli
described by Macfie and Ingram.
Larva (figs. 1-3). A very small larva, this variety being of the
same size as funestus.
Inner clypeal hairs long and simple ; outer much shorter and
branched, the number and arrangement of the branches somewhat
variable (see fig. i, A, A'), Posterior clypeal hairs minute and
simple or with bifid ends ; these are much shorter than those in
var. freetownensis and are more anteriorly situated. Antenna with
spiculated inner surface and minute hair towards the base ; hair
at apex between the two spines, dividing into three branches
(apparently two in one specimen). Mental plate with the lateral
teeth very uneven ; those nearest to the apical tooth much smaller
415
4i6
than the next teeth (fig. i, B). Anterior submedian thoracic hairs
arising from a common but not well-chitinised base ; the hairs are
somewhat variable but show no marked difference from those of
A. marshalli var. freetownensis. Metathorax with a pair of palmate
bristles with narrow leaflets ending in long filamentous points as in
var. freetownensis y leaflets about fourteen to sixteen in number.
oMiMiUiriicIre
Fig. 1. A , — Clypeal hairs of larva of A.
another specimen of same j Z?. — Mental plate c
freetownensis. B and C drawn to same scale,
drawn with the aid of a camera lucida.
marshalliy var. moucheti ; A ' . — Outer clypeal hair of
f same j C . — Mental plate of larva of A. marshalli, var.
The essentials of these and the following figures were
Abdominal tergal plates larger than those of var. freetownensis
but not nearly so large as those of funestus (fig. 3). Palmate bristles
present on abdominal segments one to seven, that of the first
segment rudimentary, the leaflets not so well developed as in var.
freetownensis (fig, 2, A, B). Palmate bristles on remaining segments
slightly smaller than in var. freetownensis, the leaflets being slightly
narrower and the filaments relatively much longer than in that
variety (C, D). Lateral comb much as in vds' freetownensis, the
barbs on the teeth rather indistinct in the specimens.
This larva differs from those of A, marshalli from South Africa
and its variety freetownensis, chiefly in the definitely branched outer
clypeal hairs and in the relatively longer fil^ents of the abdominal
417
Fig. 2. A . — A few leaflets from median part of palmate bristle of first abdominal segment of
larva of A. marshalli^ var. freciownensis ; B. — The same of var. moucheti ; C .- — The same of the
fifth abdominal segment of var. freetownensis ; D. — The same of var. moucheti.
Fig. 3. Tergal plates of abdominal segments 5 to 8, as indicated. A. — A. marsballi^ var.
frtetoumgnsis ; B. — var. moucheti ; C. — A. funestus.
palmate bristles. It also differs from var. freetownensis in the very
short posterior clypeal hairs and other characters noted above and
illustrated in figs. 1-3, and from typical marshalU in the finely-
pointed leaflets of the thoracic palmate bristles. The larva described
as that of A . marshalU, by Ingram and Macfie, from the Gold Coast,
differs very greatly from the three above-mentioned larvae in having
no rudimentary palmate bristles on the thorax or first two abdominal
segments, and the palmate bristles on the other segments are com-
posed of leaflets which ' show no shoulder and scarcely any filament.'
Pupa (figs. 4, 5). The pupa is about equal in size to that of
funestus.
o-57rnlliftr!rL>
Fi<j. 4.. Pupal respiratory trumpets. A, and B. — A. tnarshalli, var. moucbeii, showing two
typical aspects ; C, — var. freetownensis ; D. — var. hargreavesi.
The respiratory trumpets (fig. A, B) are open to the base at
one point, so that, although there is a small basal continuation,
below the level of the opening, there is no true ' meatus ' or tubular
portion. Probably in consequence of this, the trumpets are often
flattened out when mounted, as shown in fig. 4/ B.
419
Abdominal chaetotaxy (fig. 5, A). The lateral bristles (1), on
segments four to seven, of the usual spine-like form, very short on the
third segment and reduced to a minute tubercle on the second ;
on the eighth segment these bristles are fringed as usual, and are
about one-fifth to one-sixth the length of the paddles. The sub-
median series (5W.), well developed and branched on the second
Fig. 5. A . — Abdomen of pupa of A. marsballi^ var. moucheti^ except first three segments, dorsal
aspect ; B . — Fifth abdominal segment of pupa of var. bargreavesi ; C. — The same of var.
freetawnensis ; a.sm. — anterior submedian bristle ; /. — lateral j si. — sublateral j sm. — submedian.
to the fourth segments, but as usual, more strongly developed on
segments five to seven, where they form a strong tuft of 6 to 8
branches arising from a short steni. Sublateral series (s/.), well
developed and branched on segments three to seven, consisting of
3 to 5 branches on the last four of these. Anterior submedian
branched hairs (a.sm.), well developed and consisting of 3 to 5
branches on the fourth to seventh segments. Paddles of the type
420
broa<iiy expanded distally, witJn fringe only on the outer side of the
apical bristle, with well-developed ‘ buttress ' along the basal part of
the outer ^ide and apical bristle of the angularly hooked shape ; sub-
apical hair very slender, usually 3-branched, the stem about equal
in length to the branches. Fringe short and spine-like on the lateral
margin, longer and hair-like on the distal margin, the change from
one type to the other abrupt.
Described from one larval pelt and two larvae and numerous pupal
pelts, taken from a pool (‘ Etang de la Mission, rive herbeuse ') ;
and streams (' ruisseaux, herbes a sol *), August and September,
1928, Dr. J. Schwetz. Adults of typical A. marshalli var. moucheti
were bred from the pelts.
Variation in female palpal markings. In two of the bred
out by Dr. Schwetz, the palpi were entirely without the subapical
dark ring, the whole of the outer third of the palpi being white-
scaled.
Male ierminalia. The claspers have the usual five parabasal
spines which are similar in character to those of funestus, as illustrated
by Christophers (1925). The lobes at the bases of the side pieces
(harpagones, Christophers, 1915) with the apical bristle longer
than the club and a shorter bristle externally. Phallosome or
mesosome (fig. 6 , B), with four or five leaflets at each side of the tip.
Longest pair of leaflets much longer than those next to it and slightly
serrated at the base.
Described from seven specimens, four of which were stained
with carbol fuchsin ; all were mounted so as to display the mesosome.
ANOPHELES MARSHALL! var. HARGREAVES! Evans
Amongst the material sent by Dr. Schwetz was a perfectly
preserved female, with its pupal pelt, of a variety of marshalli
which agreed extremely closely with that of var; hargreavesi from
Sierra Leone, In the banding of the palps and tarsi and shape and
size of the wing scales, the Congo specimen is indistinguishable from
that variety. The third and fourth dark costal spots are somewhat
greater in extent than in the type of hargreavesi, but in this they agree
with a specimen of hargreavesi from Southern Nigeria, The thoracic
4ai
scales are of the broad type, much broader than in any other variety
of marshalli, but not quite so broad or with such a large proportion
of truncate scales as in the type of hargreavesi. From a study of
four other West African specimens, three of which are Nigerian,
there is little doubt, however, that Dr. Schwetz's specimen is within
the limits of variation of that variety.
It should be noted here that the wing scales of var. hargreavesi are
indistinguishable in size and shape from those of var. moucheti,
and that the presence of a pale interruption in the third dark area
on the first vein (/?/), appear to be a constant character.
Pupa (figs. 4, 5). This is a small pupa about equal in size to
that of var. moucheti.
The respiratory trumpets appear to have a very short meatus,
as shown in fig. 4, Z), but the wall at the base of the opening is so
thin that it is difficult to be certain how far the opening extends.
The abdominal chaetotaxy differs from that of both var. moucheti
and freetownensis, but the lateral series are very similar to those
of the former. The submedian series are 3-branched on the second
segment and longer and 3- or 4-branched on the third ; on the
fourth segment they are almost as well developed as on the fifth,
and are a 2-branched bristle on one side, a 3-branched on the other.
On the fifth to the seventh segments these are long, double bristles,
as long as the tergites. The sublateral series on the fourth to sixth
segments are long as in var. moucheti, but do not show more than
three branches. The anterior submedian hairs have also fewer
branches than in var. moucheti, having 3 branches where, in that
variety, there are 5. The paddles have the distal margin appearing
much less rounded internally than in var. moucheti ; the fringe
resembles that of moucheti in that there is a very sharp demarcation
between the spine-like processes and the more distal hair-like
processes. The apical bristles are not complete ; the subapical
hair is bifid or trifid, the stem being about equal to the branches,
thus resembling that of var. moucheti.
Described from the pupal pelt of a specimen taken at the side
of a stream, ' herbes a sol,' Simi-Simi, near Stanleyville, Belgian
Congo, 30 August, 1928, Dr. Schwetz.
422
ANOPHELES MARSHALL I var. FREETOWNENSIS Evans
Pupa. This pupa is rather larger than that of var. moucheti
(lig. 4, A and C, fig. 5, A and C). The respiratory trumpet closely
resembles that of funestus in structure and differs from that of var.
moucheti in that the opening is not continued to the base and thus a
short tubular ' meatus ' is present, which measures about one-fifth
of the total length of the trumpet.
The abdominal chaetotaxy (fig. 5, C) differs markedly from
that of var. moucheti, but bears a good deal of resemblance to that of
funestus. Lateral series of spine-like bristles longer and rather
more slender on the fifth to seventh segments than in var. moucheti :
on eighth segment about as in var. moucheti. The submedian series
on the sedond to fourth segments are branched hairs ; on the fifth
to seventh segments these are long bristles, either single or with
2 or, occasionally, 3 branches. Sublateral series on segments five
to seven with 5 to 8 branches. Paddles differing from those of
var. moucheti chiefly as follows : Subapical hair of 4 to 7 branches
arising from a very short stem ; spine-like part of fringe only
extending a short distance and merging gradually into the fine hair-
like part ; fine processes of fringe longer than those in var. moucheti.
Apical bristles bent into a hook as in var. moucheti.
Described from the pupal pelts of eight specimens of this variety
collected in and around Freetown, Sierra Leone, 1925, by Professor
Blacklock and the writer.
Male terminalia. Five parabasal spines similar to those of
var. moucheti are usually present, but in one specimen there is an
additional short, bent, internal spine, evidently an individual
peculiarity. The lobes at the bases of the side-pieces usually have,
in addition to the bristles present in var. moucheti, a short bristle
just internal to the long one. Phallosome (fig. 6, A) with at least
six pairs of leaflets, usually eight and sometimes nine or ten. The
leaflets of each side are arranged in two or three series, the longer
ones broad and serrated and sometimes with a median thickening,
the length of the different leaflets more evenly graded than in var.
momheti.
Described from seven specimens^ iour of which were stained with
carbol fuchsin and all mounted so as to display the mesosome.
4^3
In 1927 I suggested that a study of their early stages might
throw light on the question of the status of the varieties of
A, marshalli. The larvae of the type form from South Africa
and three others are now known, and are all distinct from each
other, while of the pupae of the three varieties here described, those
of moucheti and freetownensis are easily separable from each other
and from that of the form described by Ingram and Macfie (1917)
from West Africa. The pupa here described as that of hargreavesi
Fig. 6. A . — Phallosome of A, marshalli, fre&tozvnensis ; H. — 7'hc same of var. moucheti.
is quite distinct from the former, and certainly also appears to differ
from the latter. Another larva which may possibly be that of a
variety of marshalli, was collected by the writer in a roadside ditch
in the hills behind Freetown, Sierra Leone, in 1925. In addition
to this larva, only a pupa was found in this ditch and it gave rise to a
female which agreed very closely with A . marshalli var.
domicolus Edw. The associated larva is quite different from those
of any of the forms of marshalli so far described and appears to
differ from that of any known African Anopheline larva. The
palmate . bristles are extremely small, slightly smaller than those of
costalis and only about half the diameter of those of wslv. freetownensis.
424
The leaflets are relatively much wider than in costalis and the
filaments much shorter, the proportions being about as in
freetownensis. Rudimentary palmate bristles are present on the
first two abdominal segments, but could not be detected on the
thorax which is, however, distorted owing to the fact that the
pupa was beginning to emerge. The clypeal hairs are all simple,
the outer being about two-thirds the length of the inner, and arising
some distance behind the bases of the latter. The lateral comb
is rather similar to that of freetownensis, but the five short teeth
between the lowest long teeth show a regular decrease in size from
below upwards. The pupal respiratory trumpet, which is com-
pletely developed, has a short meatus and resembles that of
freetownensis.
If this larva should prove to be that of domicolus, then that
variety would be very distinct in its larval stage from the other forms
of marshalli of which the larvae are known. It ^till remains to
be seen whether the early stages of pitchfordi, flavicosta, and austeni
are equally distinct. A good deal of confusion has existed regarding
the diagnosis of the first of these. If, however, the larvae and
pupae of specimens agreeing with the type .series from South Africa, in
having the thoracic scales almost hair-like on the posterior two-
thirds, could be compared with those of moucheti, hargreavesi and
freetownensis, it would probably be possible to define more clearly
the characters of this variety. The differences which are shown to
exist between the male terminalia of the two varieties, mouoheti
and freetownensis, suggest that a study of these structures in other
varieties might afford another clue to the limits of variation and
relationships of the forms of marshalli. It seems possible that one
or more new forms may have to be regarded as distinct, or that some
of the existing varieties be raised or re-raised to specific rank. It is
obvious, however, that a thorough examination of the early stages
and male terminalia of series of specimens showing many shades of
variation will have to be made before a definite conclusion can be
reached.
4*5
REFERENCES
Blacklock, B., and Evans, A. M. (1926). Breeding places of Anopheline mosquitos in and around
Freetown, Sierra Leone. Ann. Trop. Med. & Parasitol., 20, 59-
Christophers, S. R. (1915). The male genitalia of Anopheles. Ind. Jl. Med. Res.^ 3 , 371.
Evans, A. M. (192$)- A new variety of Anopheles marshalli Theobald, from the Belgian Congo.
Ann. Trop. Med. & Parasitol.y 19, 21 1.
(*925)« A new variety of Anopheles marshalli from Sierra Leone. Ann. Trop. Med. and
Parasitol.^ 19, 461.
(1927)- A short illustrated guide to the Anophelines of Tropical and South Africa. Liverpool
School of Tropical Medicine Memoir^ New Series, No. 3, 1-78.
Ingram, A., and Macfie, J. W. S. (1917). Notes on some distinctive points in the pupae of West
African mosquitos. Bull. Enl. Res., 8 , 73.
(1917). The early stages of certain West African mosquitos. Bull. Ent. Res., 8 , 133.
Macfie, J. W. S. (1919). The chaetotaxy of the pupa of Stegomyia fasciata. Bull. Enl. Res.^ 10, 161.
DE Meillon, B. (1928). Notes on some mosquitoes found in South Africa. No. i. South Afr. Jl.
Sci., 25, 316.
Volume XXIII
December 31, 1929
No. 4
ANNALS
OF
TROPICAL MEDICINE AND
PARASITOLOGY
ISSUED BY
THE LIVERPOOL SCHOOL OF TROPICAL MEDICINE
Edited by
Professor WARRINGTON YORKE, M.D., M.R.C.P.
Professor D. B. BLACKLOCK, M.D.
Professor W. S. PATTON, M.B.
Emeritus Professor R. NEWSTEAD, E'.R.S.
THE INCORPORATED
LIVERPOOL SCHOOL OF TROPICAL MEDICINE
Founded by Sir ALFRED LEWIS JONES, K.C.M.G.
(Affiliated with the University of Liverpool)
Hon. President: H.R.H. The Duke of York, K.G., G.C.V.O.
Chairman : Sir F. C. Bowring.
Vice-Chairmen: Mr. H. D. Dickie
Professor E. W. Hope, O.B.E., D.Sc., M.D.
Hon. Vice-Presidents : The Earl of Derby, K.G., G.C.V.O., C.B., LL.D.
Baron Kylsant, G.C.M.G.
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Mr. 0. Harrison Williams
COMMITTEE
Vice-Chancellor H. J. W, Hetherington, )
M.A., LL.D. j
Mr. H. Wade Deacon, C.B.E. )
Associate Professor W. J. Dilling J
Professor J. M. Beattie, M.A., M.D., i
C.M., M.R.C.S., L.R.C.P.
Professor W. Ramsden, M.A., D.M., B.Ch.)
Mr. Enfield E. Fletcher
Mr. J. N. Sellers
Mr. Cecil Bates
Mr. G. Brocklehurst
Mr. J. R. Danson
Mr. R. D. Holt
Mr. David Jones
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Mrs. Percy F. Kipling
Mr. R. Rankin
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Mr. O. Harrison Williams
Professor W. Yorke, M.D., M.R.C.P.
Professor D. B. Blacklock, M.D.
Professor W. S. Patton, M.B.
University of Liverpool
Council of University of Liverpool
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Pembroke Place, Liverpool
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staff, 1929
Alfred Jones Professor of
tropical Medicine . . WARRINGTON YORKE, M.D., M.R C.P.
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Entomology . . . . WALTER SCOTT PATTON, M.B.
fV alter Myers Professor of
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Professor of Tropical Diseases of
Africa .... N’acant.
Lecturer on Entomology , . ALWEN M. liVANS, D.Sc.
Assistant Lecturer on Entomology . Vacant.
Lecturer on Protoxoology . . A. R. D. ADAMS, M.D.
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Royal Infirmary, Liverpool
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The Manaos Research Laboratory
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T. H. DAVEY, M B.
VI
THE MARY KINGSLEY MEDAL
This medal was struck in commemoration of the work of the late
Miss Mary Kingsley in West Africa, and is conferred in recognition
of distinguished scientific achievement.
HONORARY RECIPIENTS
Her Royal Highness Princess Christian
Lord Lister
The Right Hon. Joseph Chamberlain
Prince Auguste d’Arenberg
Mrs. Pinnock
Mr. William Adamson
Professor William Carter
RECIPIENTS
1905 --
Colonel Sir David Bruce, K.C.B.
Geheimrath Professor Robert Koch
Dr. A. Laveran
Sir Patrick Manson, K.C.M.G.
1907 —
Professor Danielewsky
Dr. Charles Finlay
Mr. W. M. Haifkine
Professor Golgi
Colonel Gorgas
Professor Theobald Smith
1910 —
Sir William Macgregor, G.C.M.G.
Professor R. Blanchard
Dr. Anton Breinl
Professor Angelo Celli
Dr. C. W. Daniels
Surgeon-General Sir Alfred Keogh
Colonel W. G. King
Professor Nocht
Professor G. H. F. Nuttall
Major Leonard Rogers
Professor J. L. Todd
Surgeon-General Walter Wyman
1913 —
Professor Fred. V. Theobald
1917 —
Dr. Griffith Evans
1919 —
Dr. J W. Scott Macfie
The Oswaldo Cruz Institute, Rio de
Janeiro
1920 —
Major E. E. Austen, D.S.O.
Dr. A. G. Bagshawe, C.M.G.
Dr. Andrew Balfour, C.B.
Dr. A. L. G. Broden
Mrs. Chalmers, in recognition of the
work of the late Dr. A. J. Chalmers
Professor B. Grassi
Professor R. T. Leiper
Professor F. Mesnil
Dr. Edmond Sergent
Dr. C. W. Stiles
Dr. T. Zammit
1929
Dr. G. Carmichael Low
Dr. G. A. K. Marshall, C.M.G.
Professor R. Newstead
Dr. A. T. Stanton, C.M.G.
Professor J. W. W. Stephens
Dr. C. M. Wenyon, C.M.G., C.B.E.
Vll
THE ALAN H. MILNE MEDAL
This medal was struck to commemorate the late Alan H. Milne,
C.M.G., the first Honorary Secretary of the School (1899-1917), and
is awarded twice yearly on the recommendation of the examiners
for the Diploma in Tropical Medicine.
1921—
George Phillip Farmer Allen*
1922— -
Quintin Stewart
1923—
John Cecil Cruickshank
1926—
John McPhail Campbell
Triloki Nath Varma
1927—
Alexander M. Gillespie
Joseph Hector Pottinger
Ragade Sanjiva Rao
1924—
George Maclean
Frederick John Carlyle Johnstone
Bernard Langridge Davis
1925—
Khwaja Samad Shah
Alfred Robert Davies Adams
Alfred J. Hawe
1928 —
Joseph Fine
1929—
Robert Erskine Anderson
Aubrey Vernon Greaves
Ian Cameron Middleton
VI 11
NOTICE
The following courses of instruction are given by the Liverpool
School of Tropical Medicine each year : —
(1) Two courses for the Diploma in Tropical Medicine,
commencing on the ist October and the 6th January.
The D.T.M, examinations are held in December and
March.
(2) Two courses for the Diploma in Tropical Hygiene,
commencing on the 13th January and the 23rd April.
The D.T.H. examinations are held in March and July.
(3) Two courses in Veterinary Parasitology, commencing on
1st October and the 7th January.
DIPLOMA TN TROPICAL MEDICINE
This Diploma shall be awarded only to candidates who possess
a qualification to practise Medicine recognised for this purpose by
the University, and who present satisfactory certificates of having
attended approved courses of study, and pass the prescribed
examination.
DIPLOMA IN TROPICAL HYGIENE
This Diploma can only be taken by those who have already
obtained the D.T.M. of the University of Liverpool.
' The course for this Diploma will not be conducted unless
at least live applications are received, and no application for
admission can be considered later than December 21st and
March 31st respectively.'
FEES
D.T.M. Course
D.T.H. Course
Course in Veterinary Parasitology
Each Diploma Examination
... Twenty Guineas
... Ten Guineas
... Fifteen Guineas
... Five Guineas
Fee for use of a School microscope during one term ... One Guinea.
For prospectus and further information, application should be
made to the Hon. Dean, School of Tropical Medicine, University of
Liverpool.
IX
The following have obtained the Diploma in Tropical Medicine
of the University of Liverpool : —
Diploma in Tropical Medicine
Date oj
Diploma
1904 Augustine, Henry Joshua
1904 Bennett, Arthur King
1904 Bruce, William James
1904 Byrne, John Scott
1904 Clayton, Thomas Morrison
1904 Dalziel, John McEwen
1904 Dee, Peter
1904 Greenidge, Oliver Campbell
1904 Hehir, Patrick
1904 Khan, Saiduzzafor
1904 Laurie, Robert
1904 Maclurkin, Alfred Robert
1904 McConnell, Robert Ernest
1904 Nicholson, James Edward
1904 Philipson, Nicholas
1904 Sharman, Eric Harding
1904 Thomson, Frank Wyville
1904 Walker, George Francis Clegg
1905 Anderson, Catherine Elmslie
1905 Brown, Alexander
1905 Caldwell, Thomas Cathcart
1905 Critien, Attilio
1905 Hooton, Alfred
1905 Hudson, Charles Tilson
1905 Illington, Edmund Moritz
1905 Macfarlane, Robert Maxwell
1905 Maddock, Edward Cecil Gordon
1905 Moore, James Jackson
1905 Nightingale, Samuel Shore
1905 Radcliffe, Percy Alexander Hurst
1905 Young, John Cameron
1906 Adie, Joseph Rosamond
1906 Arnold, Frank Arthur
1906 Bate, John Brabant
1906 Bennetts, Harold Graves
1906 Carter, Robert Markham
1906 Chisholm, James Alexander
1906 Clements, Robert William
1906 Dundas, James
1906 Faichnic, Norman
1906 Jeffreys, Herbert Castelman
1906 Mackenzie, Donald Francis
1906 Pailthorpe, Mary Elizabeth
1906 Palmer, Harold Thornbury
1906 Pearse, Albert
1906 Sampey, Alexander William
1906 Smithson, Arthur Ernest
1906 Taylor, Joseph van Someron
1906 Taylor, William Irwin
1906 Tynan, Edward Joseph
1906 Watson, Cecil Francis
1906 Willcocks, Roger Durant
1906 Williamson, George Alexander
1907 Allan, Alexander Smith
1907 Allwood, James Aldred
1907 Bond, Ashton
1907 Branch, Stanley
Date of
Diploma
1907 Coliinson, Walter Julius
1907 Davey, John Bernard
1907 Donaldson, Anson Scott
1907 Fell, Matthew Henry Gregson
1907 Gann, Thomas William Francis
1907 Graham, James Drummond
1907 Iliscock, Robert Carroll
1907 Keane, Joseph Gerald
1907 Kennan, Richard Henry
1907 Kenrick, William Hamilton
1907 Le Fanu, George Ernest Hugh
1907 Mackey, Charles
1907 Maddox, Ralph Henry
1907 McCarthy, John McDonald
1907 Raikes, Cuthbert Taunton
1907 Ryan, Joseph Charles
1907 Vallance, Hugh
1908 Caverhill, Austin Mack
1908 Crawford, Gilbert Stewart
1908 Dalai, Kaikhusroo Rustomji
1908 Dansey-Browniiig, George
1908 Davidson, James
1908 Dickson, John Rhodes
1908 Dowdall, Arthur Melville
1908 Glover, Henry Joseph
1908 Greaves, Francis Wood
1908 Goodbody, Cecil Maurice
1908 Harrison, James Herbert Hugh
1908 Joshi, Lemuel Lucas
1908 Le Fanu, Cecil Vivian
1908 Luethgen, Carl Wilhelm Ludwig
1908 Mama, Jamshed Byramji
1908 McCay, Frederick William
1908 McLelJan, Samuel Wilson
1908 Pearce, Charles Ross
1908 Schoorel, Alexander Frederik
1908 Smith, John Maegregor
1908 Stewart, George Edward
1908 Tate, Gerald William
1908 Whyte, Robert
1909 Abercrombie, Rudolph George
1909 Allin, John Richard Percy
1909 Armstrong, Edward Randolph
1909 Barrow, Harold Percy Waller
1909 Beatty, Guy
1909 Carr-White, Percy
1909 Chevallier, Claude Lionel
1909 Clark, William Scott
1909 Cope, Ricardo
1909 Fleming, William
1909 Hanschell, Hother McCormick
1909 Hayward, William Davey
1909 Henry, Sydney Alexander
1909 Innet, Francis Alexander
1909 Jackson, Arthur Frame
1909 Kaka, Sorabji Manekji
1909 McCabe-Dallai, Alfred Alexander Donald
X
Date of
Diploma
1909 Meldrum, William Percy
1909 Murphy, John Cullinan
1909 Samuel, Mysore Gnananandaraju
1909 Shroff, Kawasjee Byramjee
1909 Thornely, Michael Harris
1909 Turkhud, Violet Ackroyd
1909 Webb, William Spinks
1909 Yen, Fu-Chun
1910 Brabazon, Edward
1910 Castellino, Louis
1910 Caulcrick, James Akiiade
1910 Dowden, Richard
1910 Haigh, William Edwin
1910 Hamilton, Henry Fleming
1910 Hefferman, William St. Michael
1910 Hipwell, Abraham
1910 Homer, Jonathan
1910 Houston, William Mitchell
1910 James, William Robert Wallace
igio Johnstone, David Patrick
1910 Korke, Vishnu Tatyaji
1910 Macdonald, Angus Graham
1910 Macfie, John Wm. Scott
1910 Manuk, Mack Walter
1910 Murison, Cecil Charles
1910 Nanavati, Kishavlal Balabha
1910 Nauss, Ralph Welty
1910 Oakley, Philip Douglas
1910 Pratt, Ishmael Charles
1910 Sabastian, Thiruchelvam
1910 Shaw, Hugh Thomas
1910 Sieger, Edward Louis
1910 Sousa, Pascal John de
1910 Souza, Antonio Bernardo de
1910 Waterhouse, John Howard
1910 White, Maurice Forbes
1911 Blacklock, Donald Breadalbane
1911 Brown, Frederick Forrest
1911 Chand, Diwan Jai
19 1 1 Holmes, John Morgan
1911 levers, Charles Langley
1911 lies, Charles Cochrane
1911 Ingram, Alexander
1911 Kirkwood, Thomas
1911 Knowles, Benjamin
1911 Liddle, George Marcus Berkeley
1911 Lomas, Emanuel Kenworthy
191 1 Mackarell, William Wright
1911 MacKnight, Dundas Simpson
1911 Mascarenhas, Joseph Victor
1911 Murray, Ronald Roderick
1911 Oluwole, Akidiya Ladapo
1 91 1 Rao, Koka Ahobala
1 91 1 Sin ton, John Alexander
1 91 1 Tarapurvalla, Byramji Shavakshah
1911 Taylor, John Archibald
1911 Woods, William Medlicott
1912 Aeria, Joseph Reginald
1912 Anderson, Edmund Litchfield
1912 Borle, James
1912 Bowie, John Tait
1912 Brasiey, Laurence Percival ;
Date of
Diploma
1912 Christie, David
1912 Dillon, Henry de Courcy
1912 Dunn, Lillie Eleanor
1912 Hardwicke, Charles
1912 Jagose, Jamshed Rustomji
1912 Kochhar, Mela Ram
1912 McGusty, Victor William Tighe
1912 Milne, Arthur James
1912 Mitra, Manmatha Nath
1912 Myles, Charles Duncan
1912 Pelly, Huntly Nevins
1912 Prasad, Bindeshwari
1912 Prentice, George
1912 Ross, Frank
1912 Russell, Alexander James Hutchison
1912 Ruthven, Morton Wood
1912 Sandilands, John
1912 Seddon, Harold
1912 Smalley, James
1912 Strickland, Percy Charles Hutchison
1912 Watson, William Russel
1913 Austin, Charles Miller
1913 Banker, Shiavux Sorabji
1913 Becker, Johann Gerhardus
1913 Carrasco, Milton
1913 Clark, James McKillican
1913 Forsyth, Charles
1913 Grahame, Malcolm Claude Russell
1913 Grieve, Kelburne King
1913 Hargreaves, Alfred Ridley
1913 Hepper, Evelyn Charles
1913 Hiranand, Pandit
1913 Jacksan, Oswald Egbert
1913 Khaw, Ignatius Oo Kek
1913 MacKelvie, Maxwell
1913 MacKinnon, John MacPhail
1913 Macmillan, Robert James Alan
1913 Mouat-Biggs, Charles Edward Forbes
1913 Noronha, John Carmel
1913 O'Connor, Edward
1913 OIubomi-Beckley, Emanuel
1913 Pestonji, Ardeshir Behramshah
1913 Puttanna, Dodballapur Sivappa
1913 Reford, John Hope
1913 Smith, Edward Arthur
1913 Stewart, Samuel Dudley
1913 Walker, Frederick Dcarden
1913 Wilbe, Ernest Edward
1913 Wilson, Hubert Francis
J913 Yin, Ulg Ba
1913 Young, William Alexander
1914 Arculli, Hassan el
1914 Chohan, Noormahomed Kasembha
1914 Connell, Harry Bertram
1914 Gerrard, Herbert Shaw
1914 Gimi, Hirji Dorabji
1914 Gwynne, Joseph Robert
1914 Hodkinson, Samuel Paterson
1914 Jackson, Arthur Ivan
1914 Kaushash, Ram Chander
1914 Kelsall, Charles
1914 Luanco y Cuenca, Maximino
1914 Misbah, Abdul'Ghani Naguib
XI
Date of Date of
Diploma ^ Diploma
1914 Naidu, Bangalore PasupuIatiBalakrishna 1921 Nixon, Robert
1914 Rowe, John Joseph Stephen
X914 Roy, Raghu Nath
1914 Shiveshwarkar, Ramchandra VUhnu
1914 Sur, Sachindra Nath
1914 Talati, Dadabhai Cursedji
£914 Wilkinson, Arthur Geden
1914 Wright, Ernest Jenner
1915 Lobo, John Francis
1915 Madhok, Gopal Dass
1915 Pearson, George Howorth
1915 Swami, Karumuri Virabhadra
1915 Wood, John
1916 Barseghian, Mesroob
1916 Chaliha, Lakshmi Prasad
1916 Lim, Albert Liat Juay
1916 Lim, Harold Liat Hin
1916 Metzger, George Nathaniel
1916 SSderstrom, Erik Daniel
1916 Wheeler, Louis
1917 Chapman, Herbert Owen
1917 Krishnamoorthy, Yedatore V^enkoba
1917 Lipkin, Isaac Jacob
1918 Watts, Rattan Claud
1919 Bowle-Evans, Charles Harford
1919 Burnie, Robert McColl
[919 Celestin, Louis Abel
1919 Cummings, Eustace Henry I'aylor
1919 Darling, Georgina Renington
1919 Drake, Joan Margaret Fraser
1919 Fraser, William James
1919 Gordon, Rupert Montgomery
1919 Krige, Christian Frederick
1919 Maplestone, Philip Alan
1919 Oluwole, Isaac Ladipo
1919 Rustomjee, Khusshuyee Jamesidjcc
1919 Sawers, William Campbell
1919 Thompson, Mary Georgina
1919 Turner, Gladys Maude
1919 Young, Charles James
1920 Adler, Saul
1920 Anderson, William Jenkins Webb
1920 Campbell, George
1920 Cobb, Charles Eric
1920 Cobb, Enid Margaret Mary
1920 Connolly, Evelyn Mary
1920 Fernandez, Daniel David
1920 Lim, Chong Eang
1920 McHutcheson, George Browne
1920 van der Merwe, Frederick
1920 O’ Farrell, Patrick Theodore Joseph
1920 Remner, Edowo Awunor
1920 Vaughan, James Church will
1920 Waller, Harold William Leslie
1921 Allen, George Phillip Farmer
1921 Corfield, Charles Russell
1921 Hamid, Abdul
1921 Longhurst, Bell Wilmott
1921 Macvae, George Anthony
192X Madan, Hans Raj
1921 Mulligan, William Pcrcival
1921 Richmond, Arthur Stanley
1921 Shri Kent, Shamsher Singh
1921 Skinner, James Macgrcgor
1921 Stewart, Robert Bell
1921 Thomson, Marion
1922 Bhatia, Jagat Ram
1922 Cohen, Morris Joshua
1922 Crawford, Andrew Clemmey
1922 Gilmore, Edward Raymond
1922 Gracias, Cajetan Manuel
1922 Jennings, Arthur Richard
1922 Lethem, William Ashley
1922 Paul, Sachchidananda Hoshen
1922 Pinder, John
1922 Rieley, Stanley Desmond
1922 Rutherford, Gladys
1922 Stewart, Quintin
1923 Abelman, B.
1923 Basu, Dhirendranath
1923 Cniickshank, John Cecil
1923 Doherty, Winifred Irene
1923 Edghill, Winifred M.
1923 Elsohn, John
1923 Fraser, N. D.
1923 Lee, R.
1923 Pierce, E. R.
1923 Raja, Rojaporum
1923 Reid, C. B. B.
1923 Richmond, A. E.
1923 Steven, J. B.
1923 White, Charles Francis
1924 Bilimoria, H. S.
1924 Carson, J. C.
1924 Chopra, B. I..
1924 Davis, B. I..
1924 Hardy, M. J,
1924 Jennings, C. B.
1924 Johnstone, F. J. C.
1924 Keirans, T. T.
1924 Lee, S. W. T,
1924 Macdonald, G.
1924 Maclean, G.
1924 Mathur, W. C.
1924 Mitchell, J. M.
1924 Owen, D. Uvedale
1924 Paimer-Jones, Beryl
1924 Sankeralli, E. J.
1924 Singh, H.
1924 Theron, Elizabeth M.
1925 Adams, Alfred Robert Davies
1925 Ashton, Frank Richard
1925 Ashworth, Esther
1925 Bamford, Ch'tirles Walker
1925 Beinashowitz, Jack
1925 Black, John
1925 Clark, George
1925 Coghlan, Bernard A.
1925 Collier, Ivy
1925 Crawford, E. J.
-1-925 Gumming, Patrick Grant
xii
Oats oj
/^ipltyma
1925
£llam, Mar/ Muriel
Date oJ
Diploma
1926
Rodrigues, N.
1925
Fisher, Morris
1926
Sachdev, A. S.
1925
Green, Frederick Norman
1926
Singh, B.
1925
Grutu, M. S.
1926
Singh, J.
1925
Hawe, Albert J.
Z926
Talib, S. A.
1925
Jafri, Z. H.
1926
Tan, C. L.
* 9^5
Johnstone, Eivy I.
1926
Taylor, Catherine F.
1925
Kerr, James R.
1926
Turnbull, N. S.
J925
Mackay, Donald M,
1926
Turner, J. G. S.
*925
Mackay, E. K.
1926
Vardya, B- K.
J925
Makkawi, M.
1926
Varma, T. N.
1925
Maldonado, Leopoldo Garcia
1926
Voigt, C.
*925
Mar, Severo Francisco
1926
Wasti, S. N,
1925
1925
Mozoomdar, B. P.
Shah, Khwaja Samad
1927
APen, C. P.
1925
Skan, Douglas A.
1927
Bahl, M. I..
1925
Stone, Ernest R.
1927
Barrowman, B.
1925
Tcrrcll, C. G.
1927
Bawa, H. S.
*925
Tooth, Frederick
1927
Bilimoria, J. D.
1925
de Waal, Jacobus Johannes
1927
Burns, W. M.
1926
Aitken, W. J.
1927
1927
Daly, E. J.
Dunlop, G. A.
1926
Ashworth, A.
1927
Dyream, V.
1926
Austin, T. A.
1927
Evans, R. R.
1 926
Bansikar, R. N-
1927
Farid, M.
1926
Besson, W. W.
1927
Gillespie, A. IM.
Gunawardana, S. A.
1926
Bligh-Pcacock, R. N.
1927
1926
Bolton, Effie G.
1927
Harkness, J.
1926
Boodrie, E. H.
1927
I lay, R-
1926
Brito-Mutunayagani, IM. A. B.
J927
Hodivala, N- Al.
1926
Campbell, J. McP.
1927
Hughes, Emma
1926
Cullen, T.
1927
llyslop, Kathleen M.
1926
Davies, H, E.
1927
Ingram-Johnson, R. E.
1926
Dias, B. G. V.
1927
Kapadia, J. S.
1926
Doherty, H. A. A.
1927
Khan, F. A.
1926
Don, E. G.
1927
Khan, M. M.
1926
Earl, J. C. St. G.
1927
Labuschagne, P. N. H.
1926
Fletcher, Beatrice N.
1927
Laird, W. J.
1926
Fowler, H. P.
1927
I.ewin, B. F.
1926
Fowler, Isabella J.
1927
Macdonald, J.
1926
Hamilton, J.
1927
McElroy, R. S.
1926
Hodgkinson, Katharine M.
1927
Maclay, W. S,
1926
Jackson, R.
1927
Maguire, H. G.
1926
Kamakaka, K. H.
1927
Mahaffy, A. F.
1926
Kennedy, J. H.
1927
Malhotra, A. H.
1926
Khatri, L. D.
1927
Malhotra, A. L.
1926
Lennox, D.
1927
Manghirmalani, B. S.
1926
Lewis, A. J.
1927
Meek, A. I.
1926
McConn, C. F.
1927
Mehra, J. N.
1926
Mackay, A. G.
1927
Mehta, H. C.
1926
McLean, N.
1927
Menon, M. V.
1926
MacSweency, M.
1927
Miller, H. V. R.
1926
Malhautra, K. L.
1927
Mokand, S. N.
1926
Malik, S. B.
1927
Murgatroyd, F.
1926
Manuwa, S. L. A.
1927
Murray, A. J.
1926
Merchant, M. £.
1927
Murray, Pauline V.
1926
Mitchell, W. H.
1927
Nevin, H. M.
1926
Molony, E. F.
1927
Nirula, P. N.
1926
Nashikkar, S. G.
* 19^7
Olusoga, N. 'V.
1926
Oppenheimer, F.
1927
Parakh, D. B.
1926
Ormiston, W. S.
1927
Peters, D. O.
1926
Paterson, F, S.
1927
Peters, M. R.
1926
Patterson, F. L.
1927
Pottinger, J. H.
1926
Pouri, V.
1927
Rao, R. S,
1926
Quigley, L. D.
1927
Rodriguez, G. V. S.
1926
Robertson, A.
1927
Shah, S. R. A.
xm
Dau of
Diploma
Date of
Diploma
1927
Singh, H.
1928
Mitchell, A.
1927
Southward, J. F,
1928
Mone, R. V.
1927
Sturton, S. D.
1928
Morley, A. H.
1927
Thompson, Frances C.
1928
Mostert, H. van R.
1927
de Villiers, B. J. van de S.
1928
Mufty, S.
1927
Walkinshaw, R.
1928
van Niekerk, S. V.
1927
Wilkinson, S. A.
1928
Pandit, M. K.
1928
Ahluwalia, C. L.
1928
1928
Pearce, W. T. A.
Plum, D.
1928
Aidin, A. R.
1928
Rao, B. D.
1928
Anand, J. S.
1928
Reid, A.
1928
Askari, S. W. 11.
Beveridge, Ruby S.
1928
Sanderson, I.
1928
1928
Setna, H. M.
1928
Biswas, M. K.
Blakemore, W. L.
1928
Shearer, G.
1928
1928
Singh, B.
1928
Camps-Campins, J. M.
1928
Sivalingam, S.
1928
Chacko, M. 0.
1928
Stratton, Ella M.
1928
Chopra, A. N.
1928
Suri, R.
192S
Chaudhuri, J. P.
1928
Tuli, R. L.
1928
Choudari, K. V. R.
1928
Udvadia, F. F.
1928
Cranage, Margaret
1928
Wagle, P. M.
1928
Dhala, C. H.
1928
Wahid, A.
1928
Dhar,' K. K.
1928
Wall-Mesham, Nellie
1928
Dikshit^ H. K.
1928
Whig, P. L.
1928
1928
Everard, N. J.
Fine, J.
1929
Chakravarti, K. B.
1928
Ghei, A. N.
1929
Crawford, J.
1928
Halawani, A.
1929
Dale, W. C.
1928
Henihaw, L. E. R.
1929
Dogra, J. R.
1928
Hilmy, 1. S.
1929
Drury, G. D.
1928
Holmes, W. E.
1929
Gill, T. S.
1928
Hope-Gill, C. W.
1929
Herbertson, Margaret A. 1
1928
Kane, F.
1929
innes, J. A. L.
1928
Katial, C. L.
1929
McGregor, J. A.
1928
Khan, F. M.
1929
McQueen, W. B.
1928
Krishna, R.
1929
Majumdar, B. K.
1928
Lawrence, II. S.
1929
Middleton, I. C.
1928
Lawrence, M. R,
1929
Pearse, J. T. F.
1928
McLaren, D. W.
1929
Ramdeholl, C.
1928
Malhotra, B. D.
1929
Robinson, Elizabeth J.
1928
MalUck, B. D.
1929
Robinson, P. B.
1928
Mason, Jean R.
1929
Shafi, A.
1928
Menon, E. S. R.
1929
Verghese, T.
1928
Milne, J.
1929
Wilson, S. P.
The following have obtained the Diploma in Tropical Hygiene
of the University of Liverpool : —
Diploma in Tropical Hygiene
Date of
Diploma
1926
Aitken, W. J.
Date of
Diploma
1926
MaeSweeney, M.
1926
BHgh-Peacock, N.
1926
Oppenheimer, F.
1926
Clark, G.
1926
Skan, D. A.
1926
Collier, Ivy
1926
Talib, S. A.
1926
Cullen, T.
1926
Turnbull, N. S.
1926
1926
Davis, B. L.
Don, E. G. A.
1927
Allen, C. P.
1926
Fowler, H. P.
1927
Austin, T. A.
1926
Hawe, A. J.
1927
Besson, W. W.
1926
Lennox, D.
1927
Dunlop, G. A.
1926
Mackay, A. G.
1927
Earl, J. C. St. G.
1926
Mackay, D. M.
1927
Hamilton, J.
1926
McLean, N.
1927
Harkness, J.
XIV
Date of
Diploma
1927
Hay, R.
1927
Hyslop, Kathleen M.
19^7
Xabuschagne, P. N. H
1927
McCon, C. F.
1927
Macdonald, J.
1927
Mitchell, Winifred H.
1927
Murray, A.
1927
Nevin, H. M.
1927
Nixon, R.
1927
Ormiston, W. S.
* 9^7
Robertson, A.
1927
Walkingshaw, R.
19^ Bilimoria, J. I).
1928 Blakcmore, W. L.
1928 Choiidari, K. V. R.
1928 Dhar, K. K.
1928 Evans, R. R.
1928 Holmes, W. E.
1928 Laird, W.F.
1928 Maclay, W. S.
1928 Miller, H. V. R.
1928 Alorley, A. H.
1928 Pearson, G. H.
1928 Pottingcr, J. H.
1928 Sanderson, J.
1928 Sivalingam, S.
1928 Wilkinson, S. A.
Date of
Diploma
1929 Ahuja, S. D.
1929 Anderson, R.
1929 Askari, S. W.
1929 Booker, C. G.
1929 Bullen, W. A,
1929 Callum, E. N.
1929 Cole, H. A.
1929 Connolly, P. P. D.
1929 Cowan, J. A.
1929 Drury, G. D.
1929 Fraser, N. D.
1929 Graham-Cumming, G,
1929 Greaves, A. V.
1929 Halawani, A.
1929 Hale, G. S.
1929 Hilmy, I. S.
1929 Flowell, A. 'E.
1929 Innes, J. A. L.
1929 Latham, C. N.
1929 Lawrence, H- S.
1929 McMahon, J. E.
1929 Miller, A. A.
1929 Ramdeholl, C.
1929 Rosenbloom, A.
1929 Row, C. K.
1929 Setna H. M.
1929 Sewal, R. N.
1929 Singh, H.
1929 Talwrn-Jones, G. A.
1929 'Eurncr, H. N.
XV
ANNALS OF TROPICAL MEDICINE
AND PARASITOLOGY
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Kobinson, S. (1914). The spleen in malaria. Jinn, of Nosology,
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XVI
THE EFFECTS OF SELECTION UPON
SUSCEPTIBILITY TO BIRD MALARIA
IN CULEX PIPIENS Linn.
BY
CLAY G. HUFF*
{Department of Tropical Medicine, Harvard U Oliver sity Medical School,
Boston, Massachusetts)
{Received for publication i August, 1929)
Plates VI and VII.
INTRODUCTION
For one who is interested in the study of the biology of parasitism,
there is no better material from which to choose than one of the
malarial organisms. It has no free-living stages ; it invades the
tissues of both hosts ; and it displays a specificity of attack which
has been considered classic. The present investigations are the
result of a desire to follow the purely biological questions involved
in such a case of parasitism. Surely, there is no more interesting and
important biological problem remaining unsolved than that of the
specificity displayed by certain para.sites in the selection of their
hosts. Among such parasites the malarias are none the less
interesting biologically because of their economic importance.
The present investigations have been concerned with one aspect
of the problem of explaining the cause and nature of specificity. In
a previous publication (1927) I brought forth evidence in favour of the
existence of an individual immunity within a species of mosquito
known to be susceptible to infection. The case cited (and the one
with which we shall deal in this discu.ssion) is that of the parasitism
of Culex pipiens by Plasmodium cathemerium Hartman. As brought
out previously (1927), this avian malaria is infectious only to certain
individuals of Culex pipiens, in spite of the fact that every effort
was made to see that each individual received thousands of game-
tocytes in its infective meal. If one feeds the mosquitos upon birds
• National Research Fellow. This research was supported by a grant from the Wellington Fund.
I wish to express my gratitude to Dr. L. R. Cleveland for his interest and aid.
427
at the time when gametocytes are most numerous and, later, dissects
the mosquitos, he will find that certain individuals have escaped
infection, while the others have acquired tremendous infections.
That the uninfected ones failed to acquire the infection because of a
chance unequal distribution of parasites is an untenable hypothesis
when the massive dose is taken into consideration. A part of
Table VII is here reproduced from my previous paper (1927), to give
specific illustration of the question at hand.
Table I.
Comparison of degree of infections in the birds, with the results of the dissection of mosquitos
having fed from them. (Condensed from Table VII, p. 723, of 1927 publication.)
Lot
Parasites
per 10,000
R.B.C.
Percentage
, gametocytes
Number
gametocytes
per 10,000
R.B.C.
Total
Number
dissected
Number
positive
A
1,^13
37-^
449
IS
7
D
778
1 0.0
78
9
4
F
784
8.7
<^3
7
3
I
243
14.0
34
16
10
y
1,288
2.0
26
8
4
In that paper it was calculated (pp. 712-713) that most of these
mosquitos received several hundreds or several thousands of game-
tocytes when they took their infective meals. It seems that here is
some inherent ability to evade infection. The natural question then
arose : Is this ability of certain individuals for resisting infection
hereditary, or do environmental factors play the determining part ?
SPECIES USED AND THE REASONS FOR THEIR CHOICE
This study was conducted upon Plasmodium cathemerium, with
the domestic canary serving as vertebrate host and Culex pipiens
as the invertebrate host. Of the three species of avian Plasmodiums
available, cathemerium* was most satisfactory for this study because
• The question of the nomenclature of this species will be treated in a subsequent ^publication.
The parasite has been known in the United States as the ‘ Hartman strain * of bird malaria, and was
designated Plasmodium cathemerium by Hartman (1927b). It is the species used by the follovring
writers in the publications listed. Taliaferro (1925) called it the * recently isolated strain,* Hegner
and MacDougall (1926) did not give it a scientific ^designation,, Hartman (1927a) called it P,j>raecoXf
and Boyd (1929) has published upon it under t&e name
429
of the higher infections produced by it in the bird. Culex pipiens
was chosen as the insect host because of its preference for avian blood,
of the ease of breeding it in captivity, and of the existence of an
individual immunity already demonstrated.
METHODS EMPLOYED
The strains of mosquitos used were obtained by collecting the
larvae of adults from the field. In the case of lines and C, to be
described later, large quantities of larvae were collected from a
stagnant swamp in August, and brought into the laboratory and
bred out. Lines D and E were started from hibernating females
caught in a cellar in February, by Dr. Marshall Hertig, to whom
I wish to express my thanks at this point. Some difficulty is
encountered by either of these methods in getting this species to
breed through the first few generations. I'his is due to the fact
that only a very few of the first generation will copulate in captivity.
Many rafts of eggs will be laid but only rarely will they be viable.
However, if these are carefully nursed through the next generation
they will then usually copulate readily even in lamp chimneys and
practically all of the eggs laid will hatch.
The technique for handling the mosquitos has previously been
described (1927, pp. 712-715). The larvae were grown in large white
bowls of water to which a small amount of dehydrated blood serum
and milk powder was added daily. These bowls were kept covered
to prevent chance ovipositions from extraneous females. When
pupae appeared they were removed and placed in crystallizing
dishes over which lantern globes with gauze coverings were fitted.
The adults emerged into this globe cage and the latter was placed
over a Petri dish containing a moist cotton pad. Feeding upon
infected birds was accomplished by tying the immobilized bird upon
the top of the cage in such a manner that the mosquitos could
bite it in the pectoral region. After a lot of mosquitos had been
fed upon a .severely infected bird, the engorged ones were separated
from the unengorged and the former properly labelled and put
aside for five days. Then the females were each put into separate
oviposition chambers containing water, and given serial numbers.
As soon as ova were laid or the female died, the latter was dissected
and the stomach examined for the presence of oocysts. If the
female was infected, her progeny was kept and the above process
repeated upon it, again selecting the progeny from infected
females. Such a line was called a ' Positive * or ‘ Susceptible ’ line.
From the progeny of females showing no infection in the first genera-
tion, ‘ Negative * and ‘ Non-susceptible ' lines were begun by the
same method.
One of the most important points in this technique was the
need for feeding all mosquitos on birds with the highest possible
infections. It was especially important to make sure that the per-
centage of gametocytes was high as well as to select birds with
infections in which the total numbers of parasites were high. In
this work enough infected birds were kept on hand to provide the
desired' type of infection at the desired time. In dealing with the
negative lines of mosquitos it was necessary to run control feedings
from stock mosquitos in order to be sure that the bird upon which
they were fed possessed highly infectious blood.
All mosquitos were kept in a constant temperature room which
was equipped with thermostat and electric heater. The temperature
range was 79°-82° F. (26-o°-277° C.). The relative humidity of the
room was kept high by allowing the water to drop from the hot-water
faucet. The moisture content of the breeding cages was usually
higher than that of the room because of the use of a saturated pad
of wood-fibre cotton on the bottom of each. Inasmuch as all lots
of mosquitos were kept under identical conditions of temperature
and moisture, it is believed that these environmental conditions
could have played no differential part in the infections of the
individuals of a given lot.
It seems desirable to record here some of the difficulties which
one encounters in this type of experiment ; for it is realised that
the numbers of generations and the number of individuals in each
generation dealt with fall far short of the numbers required by those
interested purely in the genetics of the problem. First, there are
usually only about fifty to two hundred ova laid by a single female.
If all of these hatch and grow to become adults — which seldom
happens — half of them will be males. Then, when the remainder are
given an opportunity to feed upon an infected bird they often show
great indifference to the opportunity and many of them will die of
431
starvation rather than suck blood. Of those fed, a large proportion
survive long enough to allow oocysts to develop sufficiently to be
seen upon dissection. However, not all of them lay eggs, and even
some of the eggs laid are not viable. When it is remembered that
some of these larvae from the viable ova will have to be discarded
in the selection of a susceptible or non-susceptible line, it will be
seen that the vicissitudes are many and the successes few. Genetical
problems upon this line of work are ones to be undertaken by a staff
of workers rather than by an individual. It is, of course, important
to remember even in this case that one is dealing with a character
which manifests itself only in the female and that the male, therefore,
always remains an unknown factor.
The difficulties involved ought not to be blamed entirely upon
the species of mosquito used. The fact is that for mass breeding
Culex pipiens makes a splendid laboratory animal. That it is also
a good species for certain types of genetical experimentation I hope
to show in a subsequent publication, the data for which are now
nearly completed.
TABULATION OF RESULTS
An attempt has been made here to make the results obtained
as clear as possible by representing them in several different ways.
Table II gives the dissection results for the various selected lines.
After the explanation already made about the many difficulties in the
way of carrying the selection for many generations, no apology is
made for the brevity of some of the lines. It should, however, be
said in justice to the technique used, that line D came to an end
because all of the ova laid by the second generation were non- viable.
Line E was saved only by using the progeny of an uninfected mother
(from the only ova which hatched) instead of that from an infected
mother as should have been done if the latter had been available.
No males were obtained in the following generation ; so males from
B-VI were inserted, since they were the only ones available at the
time.
Figs. I and 2 present the same results in graphic form which,
it is hoped, will render a more lucid comparison of the two kinds
of strains possible. Fig. i is constructed from the actual numbers
432
Table II.
The numbers of uninfected and infected mosquitos, together with the percentages of infected
individuals in each generation, of the various strains selected from uninfected mothers, ‘ Negative,’
and from infected mothers, ‘.Positive.’
Negative
(From uninfected mothers)
Positive
(From infected mothers)
Genera-
tion
Line A
Line B
Line C
I.ine D
Line
E
Number
uninfected.
Number
infected.
Percentage
infected.
Number
uninfected.
Number
infected.
Percentage
infected.
Number
uninfected.
Number
infected.
Percentage
infected.
NumbCT
uninfected.
Number
^ infected.
Percentage
infected.
Number
uninfected.
Number
infected.
Percenwge
infected.
I
8
I
1 1
8
I
1 1
8
1 1
16
II
41
16
1 1
4*
II
20
3
13
23
*
4
3
7
70
3
29
91
2
6
75
III
28
2
7
56
0
0
37
39
51
0
0
6
41
87
IV
13
I
8
^9
0
0
0
I
0
0
0
0
23
6
21
V
3
O
o
35
0
0
0
0
0
0
0
0
0
0
VI
o
o
o
29
9
24
0
0
0
0
0
0
0
0
0
VII
0
p
o
37
6
15
0
0
0
0
0
0
0
0
0
VIII
o
o
o
3*
«
3
0
0
0
0
0
0
0
0
0
IX
o
o
o
8
2
20
0
0
0
0
0
0
0
0
0
X
o
o
o
4
0
0
0
0
0
0
0
0
0
0
74
7
8.6
250
20
7.4
48
48
50
19
40
1 67.8
43
64
59.8
Average
percentage
when first
generation
is left out.
7.5
64.8
Fig. I. Block Graph showing numbers of infected (shaded areas) individuals and uninfected
(unshaded areas) individuals in each generation.
434
of positive and negative dissections, while fig, 2 shows percentages
of the infected individuals in a given generation expressed in terms
of the total number dissected. Plate VI is an attempt to represent
graphically the pedigree of the strains. It has been possible here to
represent more clearly the origins of the various strains and to
indicate the kind of selection used. It will be seen from this figure
aiutCTSO mou u»ii«n:cT«R iwthkrs skuotsd »ftou iotsctid noDotRS
A B C D E
Fig. 2. Block Graph showing the percentages of infected individuals in a given generation
expressed in terms of the total number dissected. The dotted line shows the percentage of
individuals infected in unselected lots.
that strains A, B, and C came from the same original group of
mosquitos (from the progeny of a single female) ; and also that
strains D and E had common origins (in a group of hibernating
females). Unless otherwise shown the matings were all brother-
sister matings.
DISCUSSION OF RESULTS
In general, these results show that selection from uninfected
mothers tends to cause the percentage of individuals in the progeny
which will become infected, to be reduced ; and that selection from
infected mothers rapidly increases the percentage of individuals
susceptible to infection. Since males do not normally bite — and in
my own experience do not become infected when fed artificially
on infective blood — they remained an unknown element in the
problem and hence prevented the ready determination of the recessive
character and its subsequent isolation in a strain homozygous for it.
Lines A, B, and C had their origins in the same lot of mosquitos
435
which were fed on an infected bird and then dissected. Line A was
continued five generations, during which the inbreeding was all
brother-sister, and the selection made from uninfected mothers. The
percentage of infected individuals in any generation was never more
than 13, and the average percentage of infected individuals was
only 8*6. Line B, at this writing, has passed through ten generations.
As can be seen from the tables and figures, this line was entirely
negative to infection during the third, fourtli and fifth generations.
That these mosquitos — a total of no — failed to become infected
because of low infections in the birds is entirely disproved by the
fact that mosquitos from stock lots fed on these same birds became
severely infected. Plate VII shows an infection which was typical
of the controls. Line B was closely inbred for the first four genera-
tions, but at this stage the numbers in each lot became so small
that they had to be placed together in order to save the strain.
This, however, was followed by the unfortunate result that in the
sixth generation there was a reappearance of a fairly large per-
centage (24 per cent.) of infected individuals. Discontinuance of
this mass selection and return to close inbreeding was followed by the
result that the percentage of infected individuals decreased to
15 in the seventh, and to 3 in the eighth generation. The 20 per cent,
in the ninth generation is based upon too small a number to have
much significance. The average percentage for the whole ten
generations was 7-4. A comparison of this figure with the per-
centage of individuals which became infected when a mass lot of this
species was given an infective meal is interesting at this point.
Out of 160 random feedings from controls, using females from
larvae taken in the field, 45, or 28*1 per cent., became infected.
The results for lines C, D, and E which were selected from infected
mothers were strikingly different. After the first generation of
selection the lowest percentage of infected females in any generation
was 21, and in one case the percentage went as high as 91. The
average percentages of infected individuals were 50-0, 67*8, and 59*8,
for strains C, Z), and E respectively. These averages are strikingly
higher than the percentage of infected individuals found in mass
feeding, 28*1.
We find, then, that the number of individuals which become
infected in a given generation is closely correlated with the pedigree of
436
that stock rather than upon differences in temperature or humidity
conditions. It seems difficult to explain these results except by the
assumption that hereditary characters determine whether or not a
given individual mosquito will become infected when environmental
conditions are favourable. (It is well known that low temperatures
prevent the development of the parasites in susceptible mosquitos.)
A proof that there is operating within a species known to be
susceptible to malaria an hereditary factor which determines the
susceptibility or non-susceptibilitj’' of the individuals of that species
will, of course, explain readily the phenomenon described previously
(1927) as ' individual immunity.* On the other hand, this demonstra-
tion would seem to fit equally well in an explanation of the mechanism
of natural immunity which involves the operation of an active
resistance to infection on the part of the mosquito or in an explana-
tion which shows that failure on the part Of the mosquito host to
become infected was due to a lack of some essential nutritive agent
in its tissues. It is as easy to think of the one as being hereditary
as it is of the other. In other words, a demonstration that natural
immunity is hereditary in nature fits as well with the hypothesis
that this immunit}^ or non-susceptibility is active, as it does with that
which assumes that it is passive or atreptic.
These results ought to warn us against assuming that because
one insect has been infected by a particular parasite, all members of
that species of insect are susceptible to infection. There are very
likely many other cases in which only a small percentage of individuals
of a species is susceptible to infection with a particular parasite
and, under conditions favourable to selection, this percentage
might fall to zero or rise to one hundred. We know of at least one
other case in which this was true. While working upon the pdbrine
of silkworms, a protozoan disease caused by Nosema bombycis, Pasteur
(1870), found that although the majority of the individuals succumbed
to the infection, a few of them survived. From these individuals
which survived he started resistant stocks — a procedure which was
simpler than the one recorded in this paper because he was dealing
witb a disease of the larvae and was, therefore, able to get adults of
both sexes which had resisted the infection.
If similar conditions obtain in human malaria, a possible explana-
tion is offered of the innocuousness of a species in a malarious district
437
which is a dangerous carrier of malaria in another district. Such a
species might be represented in the former district only by a strain
composed of a low percentage of susceptible individuals ; or it is
conceivable that a race of non-susceptible mosquitos might arise
in nature from a species known to contain susceptible individuals.
The following examples are given as cases in which the existence of
biological races differing perhaps only in their susceptibility to
infection might be the explanation of the apparently innocuous
character of these species.
Covell (1927) has collected the data recorded regarding different
species of Anopheles and one of his paragraphs is here quoted in its
entirety : —
‘ One of the points brought out by the examination of the results recorded by
various observers is that a species which has been proved to be an efficient natural
carrier in one situation sometimes does not appear to play an important part in
another. An example of this is afforded by 4 . nronitiis in the Dutcli East Indies.
This species has been proved to be a good carrier of ]\ 1 .T. parasites experimentally,
and has been found naturally infected both in Malaya and in VV’estern Java. In the
latter region a sporozoite rate of 7 per cent, was recorded by Winoto. ’^"et in another
part of the Dutch East Indies, Swellengrebel and S. de Graaf dissected over 1,000
specimens with negative results, although in the same villages in which these were
caught, not only A. ludlozvi but also A. sinensis {hyreanus)^ A. harhirostris and
A. indejiiiitus (j'a^us) were found to be naturally infected. The reason for this
phenomenon has not been explained, and one can only surmise that in the latter
region the conditions were in some way unfavourable for the development of the
parasites in the former species.’
Another case differing principally because it rests upon epi-
demiological evidence but, nevertheless, being as difficult to explain,
is given in the following personal communication by Dr. Paul F.
Russell. He says : —
‘ At the Norton hydro-electric scheme in Ceylon, in October, 1925, Anopheles
maculatus mosquitoes were found breeding in abundance. Approximately a
thousand coolies had been working there for about a year and were housed at the site.
They had been recruited from various parts of Ceylon so that among them were
many gametocyte carriers. Yet an examination of the hospital records showed
that there had been no outbreak of malaria. In Malaya such a situation is not
conceivable. Wherever numbers of coolies have been housed near A. maculatus
breeding places there have always been sharp outbreaks of malaria, so that now
no project is undertaken without preliminary and coincident A, maculatus control.
For example, the new Singapore w'ater supply project at Gunong Pulai, in Johore,
is protected by extensive sub-soil draining, etc.’
In the light of what is reported here (or bird malaria and Culex
pipiens, it seems desirable to examine such cases in the future with
this in mind.
438
On the other hand, it is no more unreasonable to assume that
a species of mosquito now believed never to become infected with
human malaria — any Culicine, for example — might possibly give rise
to a strain which would be susceptible. If, in such a species, ' sus^
ceptibility ' behaves as a recessive character, it might be expected
to crop out only very rarely. We know that albino rats or crows
occur very infrequently in nature, and that when they do appear
they meet a life filled with vicissitudes which tend to exterminate
them. However, if a Culicine mosquito appeared which was capable
of becoming infected with human malaria, it is not likely that this
character would in itself be inimical to the existence of the species,
and hence it would be much more likely to remain in the hereditary
constitution of the species than albinism would be to remain in the
hereditary constitution of a rat or crow in nature. And, if such an
individual happened to be one among the few which survived a winter
or a drought in a particular region, it is certain that the number
of susceptible individuals in the race which followed would be
greatly increased. Following these facts and this line of reasoning,
it ought not to be startling to us if we should find sometime a case
in which human malaria is transmitted by Culicine mosquitos.
Bruce Mayne (1928) has shown that an Anopheline mosquito may
become infected with bird malaria. There is no evidence at present
which would preclude or even render unlikely the possibility that
if a sufficiently large number of Culicine mosquitos — perhaps
hundreds of thousands — were fed upon human garnet ocytes, one of
them would become infected. I do not wish to speculate upon the
matter. However, it seems to me that we have enough evidence
in hand to cause us to look upon the susceptibility and non-
susceptibility of mosquitos to malarias with less faith in the im-
mutability of their specificity.
SUMMARY
Selection in Culex pipiens in respect to its susceptibility or
non-susceptibility to Plasmodium cathemerium (an avian parasite)
has brought strong evidence in favour of the existence of ‘ susceptible '
and ' non-susceptible ' races in this species. Selection of progenies
from infected mothers caused the number of infected individuals in a
439
particular line to increase rapidly in percentage. Selection from
uninfected mothers caused a rapid decrease in the percentage of
infected individuals in such a line.
It is believed that this proof weakens somewhat our conception
that specificity is immutable. The proof that susceptibility and
non-susceptibility behave as hereditary characters within a species,
opens the question of whether a so-called susceptible species may
not be capable of engendering a non-susceptible race, and conversely
the question — even more important — of whether a so-called non-
susceptible race may not be able to produce a susceptible race.
REFERENCES
Boyd, G. H. (1929)- Induced vuriatious in the asexual cycle of Plasmodium cathemerium. Am, Jl.
Hyg., 9, 181-187,
CovELL, G. (1927). A critical review of the data recorded regarding the trunsmissiun of malaria by the
different species of Anopheles ; with notes on distribution, habits, and brccding-placcs. Ind.
Med, Res, Mem,,, 7, 1-117.
IIaktman, E. (1927a). Certain inter-relations between Plasmodium praccox and its host. Am. Jl.
Hyg -^ 7, 407-432.
• (*927t>). Three species of bird malaria, Plasmodium praecox\ P. cathemcrium^ n.sp., and
P. inconstans, n.sp. Arch. /, Protist., 60, 1-7. Two plates in colour.
Hegnek, R. W., and MacDougall, M. S. (1926). Modifying the course of infection with bird malaria
by changing the sugar content of the blood. Am. Jl. Hyg.^ 6 , 602-609.
Huff, C. G. (1927), Studies on the infectivity of Plasmodia of birds for mosquitoes, with special
reference to the problem of immunity in the mosquito. Am. Jl. H\g.j 7, 706-734.
Mavne, B. (1928). An Anopheline Mosquitoes [5/c.] as Host for the Parasites of Bird Malaria.
Ind.JL Med. Res.^ 16, 557-558.
Pasteur, h. (1870), Etude sur la maladies dcs \’crs a soic. (Sec (Jsuvres dc Pasteur^ 4, 1926,
Paris).
440
EXPLANATION OF PLATE VI
Diagrammatic representation of the effects of selection upon
susceptibility. The arrows indicate whether the selection was from
infected or uninfected females. The number of arrows indicates
the number of females which laid viable eggs. Designations of
generations and lines same as Figs, i and 2.
A'linals of Trop. Med. &> Parasitol., Vol. XXI II
PLATE I
C. Tinlivg &■ Co., Ltd., I
Plate VII
442
EXPLANATION OF PLATE VIl
Stomach of a mosquito from a control lot used to prove the
infectiousness of the blood of the bird.
Annals of Trop. Med. <‘^ Parasifo/., I’ol. XXI 1 1
PLATE VI
C. Tinliiig &■ Co., Lid., Im
TUNNEL RAT-TRAP FOR STORES
AND SHIPS
BY
J. A. MITCHELL, M.B., Ch R., D.P.H.
SECRETARY FOR PHHLIC HEALTH AND CHIEF HEALTH OFFICER, ONION OF SOUTH AFRICA.
{Received for puhlicati on iS June, 1929)
Plates VIII and TX.
A difficulty experienced in South Africa in dealing with forage
and grain stores and similar buildings, is that as a result of persistent
trapping, the rats sometimes become exceedingly wary and
‘ knowing,’ so that the ordinary types of trap — gin, breakback and
funnel cage — after a time prove ineffective. Another difficulty is
that it is usually impossible to lay or set traps in a store filled com*
pletely or almost so with forage, grain or similar produce, unless open
spaces and access passages have been left when the store was being
filled. Even when such stores are constructed on thoroughly rat-
proof lines^they will usually, where there is movement of produce
into and out of the store, soon be found to harbour rats among
the contents unless continuous preventive measures are taken — such
as trapping or the keeping of cats.
The Union Health Department at first studied the possibility of
providing a permanent ‘ home for rats ’ in such stores, with con-
veniently-placed openings in the floor or walls, giving access to
pipes or channels leading to fixed and permanent rat-proof chambers
conveniently placed either inside or outside the building, and provided
with facilities for shutting off at intervals the ingress or egress
channels, opening the chambers and removing the contained rodents.
Experiments with ‘ homes for rats ’ constructed on these lines were
carried out, but proved disappointing ; the system, moreover, could
only be installed in new or radically reconstructed buildings, and
entailed considerable cost.
Attention was then directed to devising some form of continuous-
acting trap which could be easily and cheaply installed in existing
stores, and left there indefinitely or for lengthy periods, even when
443
the stores was filled with produce — the rats entering it being led to a
cage trap placed so as to be convenient for inspection and removal
at intervals.
This plan was made possible by the success of Mr. W. G. Powell,
the Department’s Chief Rodent Inspector, in devising a simple and
effective ‘ valve ’ which, when placed in a tunnel or run-way used
by rats, allows them to travel in one direction, but bars their return.
This ' valve ’ consists of a stout tin or sheet-metal box, open at both
ends, measuring 7 inches long, 4 inches high and 2| inches wide,
the space between it and the sides and top of the tunnel being closed
up with wire netting, so that rats traversing the tunnel must pass
through the * valve.’ Inside the box is a little wire trap-door
7J inches long and 2 inches wide, hinged at its upper end into the
metal box an inch from the top, and with its lower end resting lightly
on the floor of the box and making with it an angle of about 25 degrees
(see Plate VIII). A rat entering this box at its upper end finds
that the little trap-door lifts lightly on its back, and passes through
the opening thus made ; the trap-door falls back into position
immediately the animal has passed through, and the rat cannot
return.
The remainder of the ‘ tunnel trap ’ is an adaptation of Powell’s
double-funnel wire-netting cage trap, a number of these traps
being arranged in series so that each opens into a common tunnel
or passage — the whole being enclosed in a narrow wooden box made
in detachable lengths, each 7 feet long, 10 inches wide and 9^ inches
high — each length having a ‘ valve ’ placed near the lower end of the
‘ tunnel.’
Each of these lengths has six openings along one side, these
being 3 inches in diameter and placed close to the floor of the box.
The openings are opposite the open ends of funnels in the wire-netting
cage enclosed in the box, the cage measuring inches wide by
8 inches high. Between the cage trap compartments in the cage is a
bait chamber which has a removable sheet-metal tray, and, at its
further end, opens directly into the ’ tunnel ’ of the cage. At each
end of the cage the tunnel ends in a small compartment extending
the whole width of the cage and communicating by a 3-inch opening
with a similar compartment in the next length of cage. The ends
of each length are fitted with catches, so that it may be securely
445
joined end to end (with the end openings opposite each other) with
the next length, or with the terminal cage trap, or the end opening
in one length may communicate with the similar opening in the next
length by means of a 3-inch metal pipe — which may be from 2 or
3 feet up to 20 or 25 feet long.
At the end of the series of lengths so connected is a single-funnel
cage trap enclosed in a detachable wooden box with hinged lid,
18 inches long and of the same cross-sectional dimensions as the
sections of the trap, namely, 10 inches by gl inches external. The
dimensions and details of construction of the cage lengths and
the terminal cage trap are shown in Plates VIII and IX. The
whole apparatus may be made by a handyman at the rate of
about one 7-foot length a day, at a cost of a few shillings for materials.
Mr. Powell has made a half-scale model for demonstration purposes,
the working of which may be interestingly and convincingly shown
with the aid of a few mice. When a rat (or a mouse, in the half-scale
model) enters one of the openings in the side of a length, it finds
itself in the wide end of a funnel which leads it into a cage compart-
ment, out of which it can escape through either of two funnels into a
bait compartment which opens directly into the tunnel at the back
of the box. Once in the tunnel it soon passes through the ‘ valve,'
is unable to return, and passes on into the next lengtli — and so on
into the terminal cage trap.
In actual trapping work, the boxed-in lengths are laid along one,
two or three sides of the store, in the angle between wall and floor,
with the openings towards the interior of the building. Suitable
bait is placed in each tray. In a forage or grain store, water and
vegetables such as potatoes, cabbage or lettuce leaves, melon-peel,
fruit, etc., will usually prove most attractive ; in buildings where
no grain is kept, wheat, barley or oats will be suitable. If water is
not near and easily available, a little in a tray will prove very
attractive. Bacon-rinds and fish also make excellent bait. The
lengths should be securely fixed end to end, with catches or screw-
nails and wire, the terminal cage trap being fixed at the lower end of
the series, and so placed as to be convenient for inspection and
removal at intervals. Care should be taken to ensure that the cage
lengths are so placed that the tunnel valves all open in the direction
of the terminal cage trap. If desired or convenient, any two cage
446
lengths, instead of being fixed directly end to end, may be joined
by a length of 3-inch piping flanged at both ends so that it can be
securely fixed by means of screw-nails over the end openings in the
cage lengths. Experience shows that rats travel readily along
such pipes. The pipes need not be horizontal, but may be sloped
so that the rats travel either upwards or downwards ; in this way
cage lengths in a first or second floor ma^^ be ' drained ’ to a cage
trap in the ground floor, or rats entering cage lengths in a cellar
or basement may be led up to the ground floor.
Trap systems of this kind have been used in forage and grain
stores for over a year past, by the Union' Health Department, in
conjunction with the Railways and Harbours Administration and
some of the large Municipalities, and have proved very convenient
and effective, especially where, as already explained, other forms
of trap have come to be ineffective. Even where most of the cage
lengths are covered with forage or grain, so that the bait trays
cannot be replenished, it has been found that the system continues
to function ; rats enter to explore, or to find safe nesting places, and
soon find their way to the terminal cage trap.
A trap system of this kind could easily be adapted and applied
to ships. The wire-netting would have to be made of some rust-
proof material, and the cage lengths, instead of being cased in wood,
should be enclosed with substantial steel plates, the top plate being
bolted on and easily removable so that the cage lengths can be taken
out and inspected at intervals. With such a trap system I feel
confident that the rat population of a vessel could be effectively
controlled and kept down to a minimum, and those remaining
might even be made use of as ‘ sentinels.' In 1925, in connexion
with the question of periodical fumigation of ships for rat destruction
purposes, I reported as follows to the Committee of the Office Inter-
national d' Hygiene Piiblique — then engaged on drafting the new
International Sanitary Convention :
‘ It is considered that in designing new ships attention should be paid to rendering
them as rat-proof as possible, and facilities should be provided for rat destruction.
The Convention should be framed so as to encourage the provision of such facilities.
If ships were constructed on rat-proof lines and provided with special chambers or
spaces, easily accessible to rats, and where they could find attractive cover and food,
but which could be easily shut off when desired and the rats therein caught and
examined, any rats finding their way oii "Board could be utilised as “ sentinels ” or
detectors of plague infection.’
447
The tunnel trap should greatly facilitate the carrying out of the
foregoing proposals. Unfortunately, no opportunity of trying-out
the system on ships in South African waters has so far occurred.
The system should preferably be installed in the ship during
construction.
I hope that the matter will be taken up and the possibilities of the
system thoroughly investigated by the British Ministry of Health
or some other National Health Authority, acting in consultation
and co-operation with the Board of Trade and Shipping Companies.
POWELL’S TUNNEL I'RAP.
MA'PERIALS AND DIRECTIONS FOR CONSTRUCI'ION.
Frame for cage and trap : No. 8 gauge galvanised wire.
Wire-Nltung : Finch (for rats) of No. 19 gauge galvanised wire.
Prongs made of pieces of 14 gauge steel wire, sharpened at one end and made to project i inch beyond
the ends of the wire-netting of which funnel is made.
Binding Wire : No. 16 or No. 18 gauge galvanised.
Trays : No. 8 sheet galvanised tin.
Boxes for cage lengths and cage trap : Pine boards, i inch (or | inch if desired ; dimensions given on
plans arc for i inch boards) ; (wo hinges, hasp lock (for cage trap) ; Screws (for fixing top of cage
lengths) ; Catches (for fixing cage lengths end to end).
Cage Lengths : 7 feet long by 10 inches wide and 9^ inches high (for t inch boards). ]''ach length
has six entrance holes — each 3 inches diameter^ and placed 4 inch above level of floor of box.
Funnels :
In Cage Trap : J.cngth, 12 inches j Diameter of aperture, at base, 8 inches; Diameter at end
of wire-netting (i inch from end), 2 inches ; Diameter at end of prongs (which project i inch
beyond wire-netting), inches.
In Trap Compartments : Length, 4 inches ; Diameter of aperture at base, 5 inches ; Diameter
at end of wire-netting, 2I inches ; Diameter at end of prongs, 2 inches.
In Tray Compartments : Length, 5 inches ; Diameter of aperture at base, 5 inches ; Diameter
at end of wire-netting, 2 inches; Diameter at end of prongs, ij inches.
In Tray Compartments and 'Perminal Cage Trap, end of funnel should be carried up cloic to the
roof oj the compartment.
448
EXPLANATION OF PLATE VIII
Plan of Powell’s Tunnel Trap. Scale : i inch to 3 feet (approximately).
Plate IX
450
EXPLANATION OF PLATE IX
Illustrating construction of Powell's Tunnel Trap.
Annals of Trop. Med. &■ ParasitoL, Vol. XXIII
PLATE 1
C. Tinling Co., Ltd., Pnp
THE DISTRIBUTION OF BLACKWATER
FEVER IN NORTH AMERICA*
BV
J. W. W. STEPHENS
[Received for publication, 6 July, 1929)
UmITI'D Statj-s.
Two Maps
Locality and Date
! Cases
Authority
G e n € r al
1820
(
1 * An article appears in the “ Medical News and
Hospital Gazette ” (? 1832) of New Orleans,
by an unknown author, in which he dates a
case of hacmaturia as far back as 1820 and in
his remarks on that and other cases, says :
“ Whether haematuria, more than epistaxis
menorrhagia or any other of the bloody
profluvia be the result of that bugaboo mias-
mata is questioned.” ’
Stamps (1886).
Arkansas, Illinois, Indiana
1837
1843
1846
encountered and treated many cases of this
disease in the Wabash and White River
bottoms in the States of Indiana and Illinois,
and from 1843 to 1846 in the White River
lowlands in the State of Arkansas, and that
in each of these localities, where I practised
at the periods named, 1 found this disease
more or less prevalent every year.’
Day (1 88 5).
General
1850
‘ The writer confidently asserts that before the
year 1850, the cases of hacmaturia, having
the remotest connection with malarial
disease, may be counted upon one’s fingers ;
whereas since that date, it has appeared
almost simultaneously from the Western
boundaries of our country to the distant
1 islands of Eastern Africa as a sporadic,
endemic and epidemic disease.’
Manson (1886).
Alabama
j
‘ Dr. R. T. Michel, an able and eminent
physician of Montgomery, Alabama, calls it
a malignant malarial fever, gives an
admirable and accurate description of the
symptoms yet, strange to say, he dates the
Smith (1900).
1867 j
history of the disease from the year 1867.’
• S'repHENS, J. W. W. (1927). The distribution of blackwatcr fever in Europe. Ann. Trap. Med. and
ParasitoL, 21 , 467.
^1928). ITie distribution of blackwatcr fever in South-West Asia. loc. cit., 22 , 53.
(1928). The distribution of blackwater fever in India, loc. cit., 22 , 170.
09 -^ 8 ). The distribution of blackwater fever in Burma and the Far East. loc. cit., 22 , 179.
(1929)* Th® distribution of blackwater fever in Africa, loc* cit., 23 , 67.
451
45 ^
United States — continued.
Locality and Date
Cases
Authority
Louisiana ...
‘ In 1886, Dr. R. H. Day read a paper before the
State Medical Society, at Baton Rouge,
Louisiana. . . . The literature of haemorr-
hagic malarial fever is very meagre and dates
back only a few years in the past.’
Louisiana ...
1843
Alabama
1845
‘ The disease was observed by a number of
physicians many years before the close of our
civil war. Among others, I may mention
Dr. C. GUdden Young, of Louisiana, 1843.
Dr. T. H. Anderson, of Mobile, Alabama,
was acquainted with the disease prior to
1850. Dr. A. G. Mabry. . . . said in
1870. . . . More than twenty-five years
ago I treated in the vicinity of Selma,
Alabama, cases of intermittent fever
presenting in a marked degree all the
symptoms characteristic of these cases at the
present day.* *
Alabama^ Arkansas,
A fississippi^ North Carolina,
Tc.xas, 1866
‘ In T'exas it showed itself first in 1866 (Ghent,
Tate, Starlcy, Hewson, Johnson (II), Heard),
and about the same time on the coast and in
the central swamps of Mississippi as far up as
Natchez (Sharpe, in the Transactions of the
Mississippi State Med. Soc. for 1874), in
Arkansas (Duval, in the Transactions of the
Arkansas State Med, Soc. for 1871) and in
Alabama, where it is very prevalent to a very
considerable extent according to accounts by
Kinnard, Scholl, Osborn, Michel, Riggs,
Hendrick, Weathcriey, Anderson, Mabry
and Webb ; and it hgs lately been reported
to occur also in North Carolina, by Raleigh
and Greene.*
Hirsch (1883).
Nnv yersey, North C arolina^
Pennsylvania
‘ The disease,* being comparatively rare in
this latitude (Pennsylvania), is sometimes
overlooked on this account.
‘ Of the seven cases which I have noted
during fifteen years, five originated in
Pennsylvania, one in New Jersey, and one in
North Carolina.*
Tyson (1883)3.
Alabama ... ... ...'
1
‘ Tvio degrees of the disease are met with, a
milder form in which other symptoms as well
as the haematuha are less pronounced and of
which instances occur in the Middle States,
as well as the South and West of ^s
1 country. Of this kind seem to be the cases
1 studied by Harley and other English
1 physicians. In addition to this, there is a
1 second more malignant form attended by
great prostration, vomiting and yellowness
of the skin, along with copious discharges of
bloody urine. Instances of the latter are
numerous in the Southern States 0! this
i.c., the milder form, possibly cases of paroxysmal haemoglobinuria.
4S3
United States — continued.
Locality and Date j
1 Cases
1
Authority
1
Alabama — continued
!
i country. . . . My attention was first called
1868
to it in September, i868, when I received
specimens of urine and the history of some
cases from i)r. R. I). Webb, of l.ivint^stoii,
Ala. . . I
General^ 1869 ‘Haemorrhagic malarial fever. . . . Syn. Boston (1869).
I Haemorrhagic Malarial Fever [Michel]. I
Hlack yaundicc ( Ghent j. Cachemia
! I Osborn j. Cachemia H acmorrbagica \
[Owens]. Jet erode Pcrtticinus Fever ;
I [McDaniel]. Malignant Congestive Fever *
I [Osborn]. Purpuraemia [Riggs.] TcUow
Remittent [Sholl]. Tello^v Disease. Cane- \
: brake Tello^v Fever. Ne:v Disease.'
Alabama^ Georgia.
Mississippi, Texas
Hare (1892) sent out questions to physicians
residing in the areas marked in the census as
having a death-rate from malaria of seventy
j per thousand or over (presumably those in
! the margin as no returns from any other
I areas are recorded).
! hifty-four of the one hundred and fifty-five
i (physicians) sec it frequently,
j 'I'he list of remedies for malarial haernaturia
{ used by the one hundred and seven
I physicians who sent replies to questions sent
out to physicians residing in the areas marked
in the census as having a death-rate from
malaria of seventy per thousand or over.
Hare (1892).
Hare an<.l Rrusen
(189;;).
Pacific Coast {Malaria)
Only the milder forms of malarial fever picvuil
on the Pacific Coast' (Washington, Oregon,
California). (Gp. under heading California.)
l»eniy (1898).
Alabama, Arkansas,
Florida, Louisiana,
Mississippi
I lacmoglobinuria from malarial disease is
frequently observed in Alabama, Mississippi,
Louisiana, Arkansas and, to a less e.xtcnt, in
Florida.
Weber (1901).
Alabama, Arkansas,
Florida, Georgia,
Mississippi, N. (.'arolina,
S. Carolina, Tennessee,
Texas, Virginia
In North .\merica, haemoghibinuric fever is
found in the Southern States, especially
parts of 'J’exas, Arkansas, Mississippi,
Tennessee, Alabama, Cieorgia, I'loricia,
N. Carolina, S. Carolina, Virginia.
Deadcrick and
'Fhompson (1916).
General {Malaria)
Trask stales ‘ that at one time malaria was
endemic over a much greater area of the
United .States than it is to-day, and in many
'Trask (1916).
sections where it is still endemic its
prevalence has greatly diminished. Fifty
years ago the disease prevailed farther north
than it docs now. The endemic area
extended to the great lakes and into Canada.
Ague was in this section the most common of
ailments and quinine the most universal of
household remedies. The early literature
indicates that the disease was formerly more
454
United States — continued.
Locality and Date Cases Authority
General (Malaria) — contd. or less prevalent also in Iowa, Minnesota, the
Dakotas, Utah, Colorado, Montana and
Wyoming.
‘ It would be of interest to explain satis-
factorily why it has all but disappeared
from Wisconsin and Michigan, two States at
one time badlv infected, and still persists in
certain sections of New England.'
‘ At the present time, there are three principal
well-recognised endemic areas, one large area
and tw'o smaller ones. The large endemic
area covers the whole South-Eastern portion
of the United States— the territory
extending from the Gulf of Mexico to a line
> north of the Ohio River, and from the
Atlantic seaboard to and into the Eastern
part of Kansas, Oklahoma and Texas. Of the '
two smaller endemic areas, one includes a
section of the Northern part of New Jersey,'
South-Eastern New York, Connecticut,
Rhode Island and part of the State of
Massachusetts. The third recognised en-
demic area is in California, and includes the
Sacramento and San Joaquin vallcvs.’
‘ I'ort Washington, Maryland, had for several
years up to 1913 the highest malaria sickness
rate of any (army) post in the United States.
In 1914 the highest rate (73 per 1,000 mean
strength) was at Washington Barracks, in the
district of Columbia. 'I'hc second highest
was at Fort Myer, \’irginia, just outside of
! Washington. . . . and the third highest at
Leavenworth, Kansas.’
Gt nt ral ‘ We know now that it is endemic. . . . in. . . . Stitt (1928).
certain of our Southern States. . . .
‘ It would seem reasonable to consider black-
water fever in the United States as secondary
to the malignant tertian infections brought
in by the slaves.’
Alabama.
Locality and Date
Cases
Authority
Alabama
’ Two degrees of the disease are met with — a
milder form in which other syniptoms as well
as the hacmaturia arc less prono^mced, and
of which instances occur in the Middle
Slates, as well as the South and West of this
country ; and second, a more malignant
form attended .. by great prostration,
vomiting, etc., yellowness of the skin, along
* with copious discharges of bloody urine.’
Tyson (1883)^.
455
At.atiama — roniinurri.
I-nca 11 ty and Date
Cases
j Authority
Alabama — rottttiintd
* While a majority of cases of malarial hacma-
turia are intermittent many arc continuous,
and of my seven cases, only two were
distinctly intermittent. One of these cases 1
published in a clinical lecture in the
I*hiladelphia Medical Times, as far hack as
j September i, 1871.’
1
im
1 ‘ My attention was first called to it in
i September, 1868, when I received specimens
of urine and the history of some cases from
Dr. R. D. Webb, of Livingston, Alabama,
who wrote also that it was not known in that
1863
part of his State, at least prior to 186^ or
1864.’
Montgomery
Deaderick and 7 'hompson (1916) state that in
Deaderick and
1869
1
March, 1869, Dr. R. J-'. Michel, of
'J'honippon (1916),
Michel (1869).
Montgomery, Ala., read a paper before the
Medical Association of the State of Alabama,
in which he spoke of the disease ‘ as a
malignant, malarial fever following repeated
attacks of intermittent, characterised by
I intense nausea and vomiting, very rapid and
complete jaundiced condition of the surf.'ice
i as well as most of the internal organs of the
body, an impacted gall bladder, and hemorr-
{ hages from the kidneys. 7 'hesc phenomena
! presented themselves in an almost unin-
terrupted link, attended by remissions and
exacerbations. It is a fever peculiar to the
United States.'
1
A malignant malarial fever following repeat ( d
American (1870).
i
attacks of intermittent, characterised by
intense nausea and vomiting, very rapid and
complete jaundiced condition of the surface
as well as most of the internal organs of the
body, an impacted gall bladder, and hemorr-
hages from the kidneys.
I'hesc phenomena present themselves in an
almost uninterrupted connection, attended
by remissions and exacerbations : the disease
is one peculiar to the Southern States, It
' has received various 8yn(jnym8 as lUack
Jaundice; Cachemia llaemorrhagica ;
Malignant Congestive Fever; Icterode
Pernicious J'ever ; Purpuracmia ; Vellow
Remittent ; Yellow Disease ; C'ane])rakc
yellow Fever, etc.
Michel (1869).
1
Greensboro ...
Deaderick and Thompson (1916) state that
Deaderick and
‘in 1867, Dr. X* C. Osborn (1868, 1870), of
'Thompson (1916).
Greensboro, Ala., observed ten cases, five of
08b(»rn (1868).
1867
1 which ended fatally, some with anuria and
Osborn (1869).
uremia. All the patients had been
[ repeatedly attacked with malaria. A few
Osborn (1870],
1869
months later his son, Dr. J. D. Osborn (1869)
read a paper before the Greensboro Medical
456
A L A B AM K—rontin ue^L
Locality and Date
(Jreemhoro — rontinufd
Sflma
1870
1845
Camden
1874
Camden
1867-1882
Cases
Society, from which it is evident that the
disease was becoming more prevalent and
that the country people were regarding it as
yellow fever.*
Deadcrick and Thompson (1916) state that
Dr. A. G. Mabry, in a report of a case of
intermitting icterode haematuric fever ....
in 1870, says, ‘ It is a mistake to suppose that
this is a new form of disease. More than
twenty-five years ago I treated in the vicinity
of Selma, cases of intermitting fever pre-
senting in a marked degree all the symptoms
characteristic of these cases at the present
day.’
Deaderick and Thompson (1916) state that
‘ Dr. McDaniel, of Camden, Alabama,
described hemoglobimiric fever in 1874, and'
says, “In calling vip my own reminiscences, I
am sure that I have occasionally, ever since
my boyhood, seen isolated cases of what was
considered intense bilious fever, with the
surfaces and under tissues stained deeply
yellow and w’ith the urine deep red. 'I'hey
were nearly all fatal and were called in older
phrase, “ ‘ bilious congestive,” ’ and in more
recent “ * pernicious bilious.” ’ 1 have also
but more rarely known groups of similar
cases associated, say three or four case.s
occurring on the same premises or in the
same family, about the same time. All such
cases in addition to the deep so-called bilious
colour and the red urine, had jactitation,
suspirous breathing, inordinate thirst and
vomiting of various shaded and tinted so-
called bilious matters. By diligently
enquiring I have ascertained that very many
old physicians, some of whom have now
retired from practice, are satisfied that they
have observed similar cases, sometimes singly
and sometimes in groups.” ’ j
‘ All the eighteen cases .... were of the type
referred to in Dr. James Tyson’s paper as
malignant baematnriay called in Alabama,
hemorrhagic malarial fever, and occurred in
the writer’s practice from 1867-1882
inclusive.’
I now present a table of 178 cases of
hemorrhagic malarial fever made up of ;
25 cases seen by myself ....
33 reported by Dr. Webb, of Livingston,
Ala.
22 reported by Dr. Sami. Perry, of Marion,
Ala.
46 reported by Dr. Jackson, ofCrecne Co.,
Ala.
Authority
Deaderick and
Thompson (1916).
Mabry (1872).
Mabry (1870).
Deaderick and
Thompson (1916).
McDaniel (1874).
McDaniel (1883).
457
A LABAM A — roniimirtl.
Locality and Date
Cases
1 Authority
Camden — continued
II reported by Dr. Webb, of Greene Co.,
Ala.
41 reported by Dr. Minor, of Greene Co.,
Ala.
Of these 178 cases :
8^ took quinine (as part of (lie treat-
ment).
93 did not take qviinine (as part of the
treatment).
Of the 85 cases with quinine :
35 or 41 per cent. died.
Of the 93 cases without quinine :
16 or 18 per cent. died.
Falkland
A statement of 41 cases (1863-1883)
Minor (1883).
Livingston ...
Analysis of 33 cases.
Webb (1883).
‘ In my account of the epidemic fever which
prevailed in 1883, in Rrewton, a small town
in Escambia County, Alabama, I have stated
in some detail the problem of differential
diagnosis which had to be solved there. 1
had for many years been familiar with yellow
Cochrane (1884).
Cochrane (i885)<7.
fever and to me it seemed perfectly clear
i that the fever at Brewton was yellow fever.
The physicians at Rrewton had been for
1 many years familiar with haemorrhagic
1 malarial fever and they asserted witli
persistent emphasis that the Brewton fever
was haemorrhagic malarial fever. . . .’
‘ In the fall of 1884 it came to my knowledge
that cases of haemorrhagic malarial fever
were recurring in several counties of
Alabama. . .
i
1
i
Lotvndes County
‘ As the result of this effort I obtained :
(i) Clinical reports of three cases, two from
Dr. S. Hopping, of Letohatchie, in Lowndes
County, Alabama, and one from Dr. R. D.
Webb, of Livingston, in Sumter County,
Alabama, which I gladly include in my
paper; (2) Several specimens of the charac-
teristic red urine. . .
1 ‘ My collection of cases numbers six hundred
and forty-tw’o (642)-- four hundred and
eighty-four recoveries (484) and one
hundred and fifty-eight (158) deaths.’
(Forty'-four replies were received in
response to one thousand letters issued
among the physicians of Alabama).
' The percentage of deaths to cases, therefore, ;
is 24.66 ; or, in round numbers, one-fourth
of the cases died, and three-fourths of them
recovered.’
‘ Black Vomit. — I took a great deal of trouble to I
secure ftdl accounts of black- vomit cases ; i
)
i
Sumter County
\
!
1
458
A LA KAMA — (ontiniied.
L<jcality and Date
Cases
Authority
Stanter ('on tit y — continiud
1
but out of the six hundred and forty-two
cases reported, only fourteen presented this
symptom and in only three cases is the black
vomit reported to have resembled coffee
grounds. It is a curious fact, too, that those
of my correspondents who have practised in
the most intensely malarial sections of the
State, and who have seen the largest number
of cases of the most malignant types, have
not seen black-vomit cases at all ; and some
of them distinctly take the position that the
so-called black vomit of haemorrhagic
malarial fever is always altered bile and not
like the black vomit of yellow fever, altered
blood.*
‘ The Red Urine. — . . . . T consider that
Dr. Sternberg’s researches have definitely
settled this question . . . . — the fact, namely,
that the red or dark discoloration of the
urine is due to the presence, not of blood,
but of the blood pigments and especially
haemoglobin — ^is also fully established for
the haemorrhagic malarial fever of Alabama/ ,
Selma
‘ About 1.30 o’clock on the morning of Dec. 15,
1885 .... This young man had had many
Riggs (1886).
attacks of this dangerous malady since child-
hood, this being the third attack since
August last, 1885. He was one of those in
whom quinine always caused “ hemorrhage
from the kidneys ” (?). '^^I’herefore I had
never been able to use the bark
derivatives. . . . His was thoroughly a case
of malarial cachexy ; he had a spleen as large
as a peck measure, hard, sore and extending
down to the crest of the left ilium and to the
the right of navel.”
‘ I have seen four cases where no quinine was
taken prior to the hemorrhage. ... Ten
successive cases without a death.’
Du Bose (1899).
General
Hare (1892) records that * In six hundred and
forty-two cases collected by Jerome
i Cochrane, health officer of Alabama, from
different practitioners, there were one
hundred and fifty-eight deaths, the death-
rate being about twenty-five per cent. . . .’
‘ Dr. T. W. Ayres, of Jacksonville, Ala., calls my
1 attention to the fact that the Report *of the
State Board of Health of Alabama^ shows
that in 1887, 1888, and 1889, there were
thirty-nine deaths from malarial haematuria,
of which twenty-five were males and
fourteen females. And he also records that,
of one hundred and eight cases, seventy-three
were males and -thwFty-fivc females.*
Hare (1892).
459
Alabama — continued.
Locality and Date
Cases
j Authority
Union Springs
‘ Twenty-five years ago the so-called hemorr-
hagic fever or malarial hematuria was one of
the most frequent and fearful diseases in this
county^ but since then it has been gradually
disappearing until it is one of the rarest
diseases. So far as I can learn, there have
been only two or three cases in the county
within the past eight years. 1 have had the
good fortune to have seen only four cases, all
of which occurred nine years ago-'-during my
first year of practice.’
Harris (1904).
‘ Haemorrhagic malarial fever as a distinct
Brockvvay (1912).
disease was unknown to the physicians of
1867
Alabama prior to 1867. True enough, there
were, scattered here and there, a few cases at
a much earlier date, but it was regarded by
the physicians of that day as a malignant
form of malarial fever. It did not attract
much attention until the year 1867, or
perhaps a little earlier, when it prevailed to
an alarming extent along the water courses of
the Southern States. Almost every com-
munity within the area was afflicted with the
terrible scourge.’
Jackson
7 (>9i^‘4)
Barber (1926).
Montgomery
2(1923-4)
‘ In 1922 I was in Southern Alabama .... and
we heard of no cases of blackwater.’
Arkansas.
Locality and Date j
Cases
[ Authority
Fort Smith |
Deaderick and Thompson (1916) state that :
Deaderick and
‘ In Arkansas, hemoglobinuric fever was first
recorded by Dr. K. R. Du \^al, ('f Fort Smith,
Thompson (1916).
in a paper read before the State Society, in
Du V^al (1871).
1871 ,
1871. He believed the case he recorded to
be the first to occur in the State.’
Monroe County ... ...'
Deaderick and Thompson (1916) state that, ‘ In
Deaderick and
1880, Dr. G. B. Malone, In Monroe County,
Thompson (1916).
Arkansas, reported 155 cases met in his
Malone (r88o) and
practice.’
(i88i).
South-West Arkansas
‘ In 1873, I commenced the practice in South-
Weathers (1886).
1873
West Arkansas, a very sickly, malarious
country, and so as chills were common, I
found that this disease was only the result of
aggravated chills or protracted cases of
malarial poison. 'Fhe doctors had never
1
1
cured a single case. . . . Well, 1 cured that
year eight out of nine on this same experi-
mental treatment.’
460
Arkansas — continued.
Locality and Date
Cases
Authority
Wallaceburg
2 cates (brother and sister) (1885)
Stamps (1886).
Bausvtlle ...
‘ Haemorrhagic malarial fever. It is always
considered dangerous. I have never seen a
case of it in the infant, and very seldom do we
see a case in our part of the State, either in
the adults or the children, however, occasion-
ally in both.’
Lawrence (1887).
IV alloceburg
‘ The majority of the cases that prove fatal
occur in rural districts, where autopsies arc
looked upon as unpardonable intrusions upon
the dead.'
Stamps (1888).
General ...
‘ A resident of Arkansas for the past five years,
the latter two having been spent on the banks
of the Red River.’
Woldert (1895).
Camden
‘ The mortality from this disease is not so heavy
as it was twenty years ago, and at that time
it was treated almost exclusively by massive
doses of quinine.’
Meek (1897).
Snyder
‘ The disease is quite common in the swamp
countries of this State, where the pernicious
forms of malaria arc most prevalent.’
II cases, I death (Feb., 1898-March, 1899)
Roop (1899).
Deckervillc ...
‘ Out of 16 cases seen by me, 13 were males and
3 females, the oldest being 38 and the
youngest years of age. Dr. McElroy, of
Stoval, Miss., shows a record of 40 cases, of
these, there were 30 males and 10
females. ... Of my 16 cases, 3 were very
light mulattoes ; of Dr. McElroy ’s 40 cases, 13
were negroes, 2 of which, he writes to me,
were full-blooded negroes.’
Burns (1900).
Marianna ...
4 (1907)
Deaderick (1908).
Hot Springs ... ...^
* Twenty-seven cases were seen in rural
residents, and seven in townspeople. . . .
All, without exception, had suffered
previously with malaria, most of them
repeatedly. ... In thirty cases, quinine
was being taken for malaria when the out-
break occurred. In four cases quinine could
be absolutely excluded.’
Deaderick (1914).
Eastern Arkansas ...
. 1
Deaderick, in Deaderick and Thompson (1916)
states that, * It is probably becoming less
frequent in some of the Southern States,
/ud£ 7 J 7 ^ from erpenence m Eastern ;
Arkansas.’ /
Deaderick and
Thompson (1916).
461
Ar KANSAS — continued.
Locality and Date
C'ases
Authority
St. Francis River Bottoms . .
‘ Dr. E. G. Fulton, Iberia : “ In the
summer of 1906, as an under-graduate, I
went over into the St. Francis River Bottoms
in Ark., got as far from the rail-road as
possible, and started in to practice medicine.
I had only been practising about two weeks
and thought I was getting along fine, when
I was called to see a case of black-water
fever.’
Wright (1917).
California.
Locality and Date
Cases
Authority
Sacramento
‘ We very rarely have cases of malarial
haematiiria here.’
Briggs (1900).
Colorado.
Locality and Date
Cases
Authority
La Grange ...
1868—9
‘ In our own country, malarial fevers, mild and
severe, have prevailed since the first settle-
ment and quinine has been extensively used
in the treatment. But malarial haematuria
is a comparatively recent disease. It w.is not
known, or but rarely met with, until since i
the close of the Civil War. I saw the disease
soon after its first appearance in the settle-
ments along the Colorado river, near La
Grange, in the years of 1868-9. • ■ •’
McLaughlin (1904).
Denver
2 cases.
Brasher (1899).
Florida.
Locality and Date
Cases
Authority
General
‘ From a rather extended experience with the
disease in question, in the State of Florida, 1
am prepared to say that all cases are amenable
to treatment by quinine^ if such treatment be
entered upon within thirty-six' hours of the
onset. ... It occurs only in those persons
who have been for a long lime subjected to
slow malarial infection without the proper
administration of quinine .... some
superficial observers jiiavc named the disease
“ highland yellow fever.” The distressing 1
symptoms are haematuria, intense n.'iusea and 1
black vomity extreme thir<it, frequently !
repeated chills of a congestive character, and, 1
at times, linking turn amounting almost to j
Stuhhert (i88h).
462
F LOR ID A — con tinned.
Locality and Date
Cases
Authority
General — continued
syncope. . . . Dr. Maxwell has met with
equally good results and in a large number of
cases. . . . The position taken by some,
that “ pure blood ” is passed from the
kidneys, seems to me untenable. ... Is it
not more reasonable to suppose that the
evacuations are urine coloured by the
colouring matter of the red corpuscles. . . . ? ^
General
'853
‘ G. Troup Maxwell, of Ocala, Florida, writes
me, in 1883, that he first observed cases in
Florida thirty years ago, and published an
article on the disease in ... . i860-’
[The possibility of confusion with paroxysmal
haemoglobinuria in early cases and others
should be borne in mind.]
Tyson (1886).
Maxwell (i860).
Leeiburgh ...
‘ This disease is getting to be a very common
occurrence in Florida, Georgia, and the
Mississippi bottoms. . . . Hemorrhatuc fever
attacks those who have previously had some
form of malarial fever. . , Records 5 cases.
Bush (1896).
Grenville
* In a number of cases that I have seen I have
been firmlv convinced that the agent which
wrought such terrific destruction with the
blood elements was not the parasite itself,
but some toxin, the existence of which
depended either on the assistance or presence
of the Plasmodium*
Greene (1905).
General
‘ Finds that nephritis is present in all cases and
influences the treatment.’
Ross (1916).
Georgia.
Locality and Date
Cases
j Authority
Dalton
Malarial haematuria. — A unique case of this
disease is recorded by Clias. P. Gordon,
M.D., Dalton, Ga., in the July number of the
Atlanta Medical and Surgical Journal . . .
‘ As there are in congestive fever the cerebral,
thoracic and abdominal varieties, he would
add another, the renal varietyj in which the
congestive tendency is to the kidneys, with
all the pernicious' results following malarial
haematuria.’ (p.£4i8).
Gordon (iSyz),
4<53
Georgia — continued.
Locality and Date
Cases
Authority
Americus
Haemorrhagic malarial fever. — At a recent
meeting of the Atlanta Academy of
Medicine, Dr. Cooper, of Americus, Georgia
(Atlanta Med. and Surg, yourn.\ called
attention to the value of large doses of the
tincture of chloride of iron in the treatment
of this variety of fever. Quinine seemed to
be of little use in this disease, (p. 187).
Cooper (1872)
Albany
‘Hemorrhagic malarial fever. — - . . . He also
remarks as a peculiarity of the disease, that
its ravages have been almost exclusively con-
fined to what is regarded as the healthiest
portion of the country — the pine woods.’
(P- 396)-
Cromwell (1872).
Americus
Deaderick and Thompson (1916) state that,
‘ the affection was first reported in Georgia,
by Dr. W. A. Greene, of Americus, in 1872.’
Deaderick and
'Thompson (1916).
Greene (1872).
Macon
‘ Concludes .... that this disease is purely
malarial.’ (p. 140).
Me Hatton (1884
and 1885-86).
Albany
’ My attention was first called to this disease in
the summer of 1884, by having a specimen of
urine referred to me for analysis. ... I
received many specimens (more from
Dr. Hillsman, of Albany, Georgia, than
from anyone else. . . .’)
McHatton (1891).
General
‘ W. Shropshire reports two cases. ... In one
instance, quinine in moderate doses had been
used in a severe case of malaria, and blood
began to be passed , in the urine. . . .
Another similar case is offered to show that
during the administration of moderate doses
of quinine, hemoglobinuria may develop.’
Shropshire (1901).
1
Colquitt County
‘ A county health officer of an adjoining
county, Colquitt, told me that in 1920
about 25 cases of blackwater had been
reported in his county.*
Barber (1926).
Mitchell County
‘ My own observation is rather meager ; in
1921 I knew of one case in Mitchell County.’
Leesburg
‘ One of the local physicians in Leesburg,
Georgia, claims to have treated blackwater
fever, with very good results, by the
administration of antistreptococcic serum.’
Boyd (1926).
Lee County
* In Lee County, Georgia, the former head-
quarters of this station (station for field
studies in malaria)- wc were located in an
area in which the endemicity was normally
not high, but which is subject to severe
visitations of epidemic malaria, at which
time cases of blackwater fever were not
uncommon.’
Boyd (1926).
Illinois.
Locality and Date
Cases
Authority
Elgin
1
‘ W. M., male, age 25, recently from a malarial
region of Kentucky and for years a victim of
that disease. . . . Dr. Bell was called and
found the patient in a delirious state,
temperature 104°. . . . The Doctor pre-
scribed quinine in large doses frequently,
sponge baths and opium as a sedative. I was ,
called a few hours later and found that the
patient had passed a very large quantity of
sanguineous urine. ... he became very
much jaundiced, the entire body being of an !
intensely lemon yellow colour.’
Gahagan (1S95).
Wetaug
‘ Malarial hematuria . — Dr. L. M. Winsted, of
Wetaug, read this paper. . . . The author *
narrated ten typical cases of the malignant
j ' type of the disease.’
Proceedings (1902).
Kentucky.
Locality and Date
Cases
Authority
JeJfcrson ('ouniy
* In a practice above the average country
1 practice around Lacona, Jefferson County,
Ky., mostly in the first bottom of the Ohio
j River, extending through all the years, from
I 1847 to and through 1875, I have met with
1 nine cases of malarial hematuria : had one
j death. ... I met with no case unless one-
! half to three-fourths of the population were
the subjects of malarial diseases, nor did ever
more than one case in a single year occur
with me, until the one that has passed, when
J met with four.’
Toss (1876).
Louisville
Askenstedt, of Louisville, contributes a paper
(presumably in reference to blackwater in
Kentucky).
Askenstedt (1912).
Louisiana.
Locality and Date
Cases
Authority
JSeu' Orleans
Deaderick and Thompson (1916) state that,
‘ Faget treated the disease as early as 1859,
Deaderick and
iSs 9
Thompson (1916),
and states that the cases with hematuria and
p. 220.
hematemesis had frequently been seen in
I Faget (1869).
New Orleans and been mistaken for yellow
fever. Inasmuch as Faget considered hema-
temesis a common symptom of hemoglo-
binuric fever, it is possible that he himself
confounded the two diseases in some
instances.’
Faget (1870).
465
LOUISIANA' — continued.
Locality and Date
Cases
Authority
Monroe ...
Deaderick and Thompson (1916) state that, ‘ In
Deaderick and
the United States hemoglobinuric fever was
Thompson (1916),
first described by Dr. J. C. Cummings, of
p. 220.
1859
Monroe, Louisiana, in 1859. lie reported
Cummings (1859-
six cases and refers to numerous cases during
the previous season.’
60).
Opelousas ...
‘ Billy Fox*, aged thirteen years, had several
paroxysms of chills and fevers. Quinine was
prescribed by the parents on tw'o occasions,
which was followed immediately (both times)
by haemorrhage from the mucous membrane
of the urinary organs- I was called (August,
Cachere (1869).
1867
1867) to see the boy and .... I prescribed
ten grains of quinine to be divided in three
doses, and to be given next day. . . . An
hour after the third dose had been
administered, the patient had a profuse
haemorrhage from the urinary passages. My
little patient was removed to Opelousas. . . .
An eminent physician of that town was
called in ... . and again quinine was
prescribed and administered, and followed
by the same kind of haemorrhage. . . . The
boy is again under my treatment, suffering
with chills and fever (tertian). Two weeks
ago, his father prescribed and administered
three or four doses of an infusion of cinchona
and Virginia snakcroot, which was followed
by haemorrhage of same organs. It has been
my misfortune to have had another similar
case last fall. To a little girl, seven years
old, quinine was administered in different
ways, but was invariably followed by
haemorrhage of the urinary passages.’
New Orleans
‘ Two cases of what he calls “ malarial haemorr-
Bemiss (? prior to
hagic fever ” in one of which he says, “ the
00
OC
urine was loaded with albumen and showed,
under the microscope, abundant blood
corpuscles ” and in the other, that the urine
was ** loaded with blood.” ’
Journal (1885).
Iberville Parish
‘ One of the complications which is beginning
to be quite common in this section is
haematuria.’
Owen (1885).
Baton Rouge
‘ It was my fortune, early in my medical career,
to become famiUar with this most terrible
disease, both in its mild and most virulent
Day (1886).
forms.*
* It is emphatically an hepatic and blood disease
of malarial origin.*
466
Louisiana — continued.
Locality and Date
Cases
Authority
General
‘ From her swamps and bayous we draw our
greater share of cases of typical malaria and
all cases of haematuria.’
Ballard (1899).
Lake Charles
‘ My experience with malarial hematuria in
private practice has been limited to nine
cases, three of which died, six recovering
entirely.*
Watkins (1901).
Ruddock
‘Out of thirty cases treated by me, twenty
were white (seventeen men and three
women) and ten were negroes (eight men,
one boy, one woman).’
M'Kay (1902).
Raccourci ...
‘ Of all the diseases with which the practitioner
in the Mississippi Delta has to contend, for
fatality none is equal to malarial haematuria.
With a mortality of fully fifty per cent., it is
not a matter of surprise that it is held in'
dread fear by the inhabitants of the region in
which it prevails. . .
‘ Histories of my first four cases. . . .’
* Rigney (1895).
General
‘ Quinine as a specijic in malarial haematuria,-^
Dr. L. G. Le Beuf read a paper at the last
meeting of the Louisiana State Medical
Society, on the subject of quinine in
haematuria, and reported four cases of the
worst type of haematuria.’
Miller (1899).
Houma
‘ 1 have treated some two hundred cases, and
have never seen a case but that had taken, in
some form, a dose of quinine, while the
system was suffering from a chronic malarial
toxaemia.’
Menville (1901).
G eneral
* Gives certain facts of his experience as regards
malarial hematuria in a swampy, wooded
region in Louisiana. . . . Quinine hemo-
globinuria is also briefly mentioned. The
parasite in the patient is the primary cause ;
quinine only acts as the provoking agent.’
Lerch (1901).
Angola
* The patient had lived in a malarial district for
the past six months ; since September, 1915,
at Angola, La., and before that time, near
Jackson, Miss.*
Ott (1916).
Monroe ...
1856
1
4 cases (1915-16)
‘ Discussion on the paper of Dr. Wright.*
Dr. Leon T. Menville, Houma: ‘According
to the latest medical history, a doctor from
Monroe, in 1856, was the first physician in
the United States to report a case of black-
water fever. . . .’
Wright (1917).
467
Louisiana — continued.
Locality and Date
Cases
Authority
Le Roy
Dr. J. T. Abshire, Le Roy : ‘ We had
plenty of it in my parish in years gone by.’
Shreveport
Dr. O. C. Chandler, Shreveport : ‘ During the
first year of my practice I had an unlucky
number of cases of blackwater fever, that is,
thirteen.’
Arcadia
At Columbia, on the Ouachita river, where
the first ten years of my professional
experience was acquired, I saw a great deal of
this disease in its most typical and malignant
form.’ Describes two cases : ‘ There seems
to be a growing belief in some sections that
there is a certain causal relation between
quinine and hemoglobinuria. . . . On the
Ouachita river . . . there was a deeply-
rooted belief among the laity, that quinine
would produce the disease ; with some it
amounted to a morbid fear and the
knowledge that they were taking the drug
during an attack, added greatly to the gravity
of the prognosis. I have seen a number of
cases myself, in which the attack developed
soon after taking large quantities of
quinine. ... I have never seen a case of
malarial hemoglobinuria in a person who did
not give a history of previous attacks of
malaria, or was profoundly under the
influence of quinine at the time of the
attack.’ (Note : the paper was written in
1903-)
Thornhill (1921)-
Mississippi.
Locality and Date
Cases
Authority
Holmes County
‘ Twenty-six years here in a miasmatic region
(the heart of the Yazoo Valley) ... It is
generally those that have had intermittent
fevers for some time and neglected these
that have or are most liable to have malarial
haematuria and among the first symptoms
are the incessant vomiting of bilious matter
and the sudden discolouration of the skin,
frequently in six hours after the onset of the
attack, and the intense yellow muddy
appearance of the eyes, while the urine is
loaded with bile and hemorrhage soon
appears, sometimes almost entirely blood
and in large quantity.*
I'hornton (1886).
i
468
Mississippi — continued.
Locality and Date
Cases
Authority
Trinity
* The mortality in my own cases, only six in
1 number, amounted to fifty per cent.’
Hamilton (1891).
T^latchez
‘ Now, as to the treatment of haematuria when |
found, 1 use ergot in half-drachm doses
every three or four hours, and strychnine
hypodermically in full doses ... I have
treated eight cases thus or about as
indicated, with no deaths.*
Ballard (1899).
Cftieral
‘ The editor of the Journal can find any number
of such cases in the Mississippi Valley,
providing he has money to induce a subject
to take a dose of quinine ; they generally
take arsenic.’
Anon (1899).
Kenoit
‘ Malarial haemoglobinuria (1 call it so to
prevent confusion with haematuria) as it
prevails in this section (the Mississippi Yazoo
Delta) is always a grave disease, the
mortality, as 1 have observed, falling but
little below fifty per cent.*
Jones (1892).
General
‘ Malarial hematuria, as its name implies,
prevails throughout the whole Southern
country, especially in all localities abounding
in lakes, swamps, stagnant water-courses,
etc.’
Jones (1894).
Stovall
‘ I have observed more than fifty cases of this
disease, and in 19 cases have made repeated
blood examinations. In only 5 of these have
parasites been present, estivo-autumnal in 4,
and double tertian in i. The malarial
nature of the remaining 14 was demon-
strated by the leucocytic variation and pig-
mentation characteristic of malaria.’
McElroy (1903).
Rosedale
ll
Sutherland (1903).
Mississippi Valley ...
Deaderick and Thompson (1916) state that :
‘ Fifty cases observed by McElroy (1905)
were distributed as follows : Two in the first
year of residence, three in the second, six
between the second and the fifth, twenty-
three between the fifth and tenth, eleven
between the tenth and twentieth, and five
after twenty years.* p. 232.
Deaderick and
Thompson (1916),
McElroy (1905).
Glarksdalc., Friar's Pointy
Hillhouse^TumiUr
‘ From 1889 to 1895, we (Dr. E. H. Marten, of
Clarksdale, and Barton, of Hillhouse)
treated sixty-eight cases without quinine,
and without a single death.*
Dr. W. H. Harrison, of Tutwiler, Miss., in
reply to a letter, writes, ‘ My experience is
against it (quinine), ^pod dnd strong. . . .
I am now actually afraid of it.* '
Buck (1906).
469
Mississippi — continued .
Locality and Date
Cases
Authority
Eaglebend ...
‘ The writer was called down in Eaglebend,
Miss., to see Roscoe Dunn (white), aged six
years, who had a malarial chill at 2 p.m. of
Aug. 23rd, 1907, turned yellow as gold
witWn two hours, and had copious
hemorrhages from his kidneys, with a
temperature of io6j degrees K. . . . The
writer was debarred from giving quinine to
prevent a recurrence of the malarial chill at
10 a.m. of August 24th, because the child’s
parents claimed that they had lost two
children, while living at Alexandria, La., by
the family physician then giving the children
sulphate of quinine. . . .’ Describes another
case and states that * Since that time the
writer has had calls to cases of malarial
hematuria. . . .’ Discussion.
Kiger (192;;).
Delta
Dr. W. H. Scudder (Maversville) : ‘ I
remember, 25 years ago, that in every
medical meeting in this State there was a
paper on hematuria, but now it seems to have
gone out of style. I am from the Delta, and
we see more of it there than you do in the
other portions of the State, and of course we
still regard it as an important disease. But
I am glad to say it is not as prevalent in the
Delta as it used to be. . . . In some parts
of Texas they call it Black Water Fever
because the urine is not red, but really is
black.’
Leflore County
‘ During two seasons, 1925 and 1926, in Leflore
County, in the delta region, wc have heard of
no cases in this county.*
‘ The older physicians here (Greenwood) and in
adjoining counties of the Mississippi delta, j
tell me that haematuria was abundant until
about 1910, when it began to diminish with
the marked diminution of malaria which took
place about that time. All agree that cases
are now rare, several of them have not had a
case for years.’
Barber (1926).
Missouri.
Locality and Date
Cases 1
Authority
St. Louis
‘ McLean reports a case of malarial hematuria j
which he considers caused by the use of 1
quinine in large doses.’ (Whether originating
in Missouri is not clear.)
* A case under observation now in the City
hospital, convalescmg from tropical malaria,
exhibits not only an enormous amount of
urobilin in the urine, but also, after precipi-
tating the urobilin, a very large amount of
hemoglobin, though the urine, when passed, j
had a normal colour.’ (Interpretation
doubtful.) '
McLean (1899).
Richter (1913).
470
New York.
Localit^r and Date
Cases
Authority
Brooklyn ...
Locality of the case not stated. (Nature of
case appears to be doubtful.)
Geiss (1900).
General
‘ Case of malarial baematuria with some peculiar
features. — Dr. Andrew H. Smith read the
history of the case (not reported). . . .
Dr. W. Gilman Thompson. . . . Certainly
haematuria in malaria affections was rare in
this part of the country. . . . Dr. A.
Alexander Smith said that within three
i years he had seen a case of malarial hacma-
turia. ... he had come originally from
the South, where malaria was prevalent.’
Medical (1897).
North Carolina.
Locality iipd Date
Cases
Authority
Edenton
‘From 15 to 25 years ago I am reliably#
informed that blackwater fever w'as very
prevalent in this section of North-eastern
North Carolina, but has probably for the past
ten years been altogether extinct in the
immediate vicinity of Edenton, although I
have learned of one death during the past
year at a point about 60 miles distant. In
this area, which is adjacent to the Roanoke
Boyd (1926).
river in Northampton County, the older
physicians tell me that blackwater fever was
1855
unknown prior to 1855, in which year the
disease made its appearance.’
Edenton
’ Hemorrhagic malarial fever. — Dr. W. A. B.
Norcom .... expressed his opinion that
Norcom (1874).
1
the disease did not, as was claimed by some,
appear for the first time a few years ago, but
that it had long been recognised .... it
either begins de novo or as the result of long or
frequent attacks of intermittent fever. . . .
It begins usually but not invariably with a
chill of about two hours’ duration, attended
with intense internal heat .... a severe
nausea is experienced, which leads to
vomiting, at first of food, then bile and then
in bad cases, of blood — the latter sometimes
resembling the black vomit. There is a
sighing respiration, insomnia, great restless-
ness, anxiety and an almost unquenchable
thirst. . . . The skin assumes a yellowish,
even a bronze colour. . . . The urine, may
simply contain large quantities of de-
generated red-corpuscles, or in severe cases,
blood and albumen. ... In severe forms
he dies, either conscious and from asthenia,
or unconscious from uraemia ; heart clot and
cholesterinemia may also cause death.’
(P- 57 I-)
471
North Carolina — continued.
I.ocality and Date
Cases
Authority
General
‘ He had received a letter from a doctor in a
town in North Carolina, asking if malarial
haematuria was frequent in the vicinity of
New York, and added that in his section it
was very frequent, occurring in from
fifteen to eighteen per cent, of all cases of
malaria.’
Medical (1897).
Kinston
‘ .... I have not considered malarial hema-
turia because it is unquestionably a different
disease from hemoglobinuria and is very
likely of an accidental origin (over-dosing
with quinine under certain conditions, etc.),
and liable to occur in almost any type of
malaria, and doubtless sometimes com-
plicates malarial hemoglobinuria.'
Parrott (1901).
General
He quotes Surgeon-General H. R. Carter, as
stating that, ‘ In the absence of statistics, I
can only say that there is much malaria in
eastern North Carolina. ... In days not
long gone by, there was a large amount of
extremely severe malaria in this section, not
less than there was in the Canal Zone, and
there is from reports not a little now,
especially blackwater fever and malaria of the
cerebral type.’
Trask (1916).
Ohio.
Locality and Date
Cases
A\ithority
Cincinnati
* A white adult male, aged 40, with frequent
attacks of chills and fever for over a year
previous to passage of blood in his urine, had
taken quinine irregularly during that time,
but had not taken any for several weeks
previous to his hematuria. Blood had
appeared constantly in his urine for two
weeks previous to his coming under my
observation, at times, he claims, almost pure
blood being passed. . . . Urinalysis :
colour light amber, and reaction sp. gr. 1010 ;
sediment reddish, amorphous and very
abundant albumin present and in con-
siderable quantities.’ (Whether blackwater
or not seems uncertain.)
1
Brown (1899).
Penksylvania.
Locality and Date
Cases
Authority
General
‘ Of the seven cases which I have noted during
fifteen years, five originated in Pennsylvania.’
Tyson (i883)tf.
Philadelphia
1
An analysis of 1,780 cases from the
Anders (1895).
Pennsylvania hospital, the Episcopal hospital,
and the Philadelphia hospital. Inhere is no
clear evidence of blackwater fever.
South Carolina,
Locality and Date
Cases
Authority
Georgetozin
‘ The disease has been familiar to the profession
Bailey (188-^).
1868
of Georgetown only in the past fifteen
years. . . . The resemblance of this disease
to yellow fever is certainly in some cases very*
striking, so much so, that it has been called
“ Swamp Yellow Fever,” but the symptoms
given above are sufficient to distinguish it.’
‘ Malarial hemoglobinuria or hemorrhagic fever
as it is called, is the result of profound
j malarial intoxication. . . .’
‘ The fall months seem to furnish many cases,
! yet it may occur at any season of the year ; I
j have seen it in the midst of winter.’
!
Sparkman (1901).
Sparkman (1905).
Tennessee.
Locality and Date |
Cases
Authority
Memphis
‘ By careful clinical study, by a large bedside
experience assisted by competent patho-
logists and microscopists, W'e have learned
that it is the product, the sum total of
neglected malaria — a malarial toxaemia. . . .
This jaundice is so pronounced that the late
Dr. Warren Stone, of New Orleans, denomi-
nated hemoglobinuria as pseudo-yellow
fever. . . . The Delta physicians, as well
1 as the laity, have learned by experience that
1 the administration of quinine with these
1 conditions present, is fraught with danger
i frequently precipitating an attack
Let me admonish you gentlemen .... not
to journey .... to South Africa to
investigate the blackwater fever, but come
South to the swamps of Arkansas, Mississippi,
and Louisiana, where* we have malaria in
Jones (1900).
abundance and in alJjafjts forms.’
473
Tennessee — continued.
Locality and Date
Cases
Authority
Memphis — continued
‘I have seen thirteen consecutive recoveries
under the “ eliminative ” treatment ; no
such record can be shown under the quinine
therapy. (Three more cases and no deaths
at time of revision of this proof.)’
Krauss (1900).
2 cases (1900) ?
Cox (1900).
‘ Last summer, during my illness, there were
admitted to St. Joseph’s hospital, 21 cases of
malarial hemoglobinuria and all were treated
with hypodermic injections of quinine ; two
recovered. On the other hand, I have now
an unbroken series of 21 cases without a
death. The main point is, avoid cin-
chonising these patients.’
Krauss (1903).
‘ Quinine has no place in the therapy of malarial
methemoglobinuria or hematuria as it is
called. ... A glance at some kidney
sections in my possession will verify this
statement. 'I'he uriniferous tubules are
blocked with granular dctrittxs, not blood-
clots, as in the hemorrhagic cases.’
Goltman (1904).
‘ It must not be inferred that the so-called
benign tertian Infections are never as8{)ciated
with pernicious symptoms, as 1 have seen
both comatose paroxysms and homo-
McT'droy (1904).
globinuria associated with these parasites.’
Texas.
Locality and Date
Cases
i
Authority
General
Deaderick and Thompson (1916) state that,
Deaderick and
‘ Dr. H. C. Ghent (1868), of Port Sullivan,
'I'hompson (1910).
1866
Texas, in 1866, reported hcmoglobinuric
fever endemic in parts of Texas.’
Ghent (1868).
‘ Dr. Ghent, of Texas, had treated forty-seven
cases, with five deaths.’
Cochrane (1885)^.
‘ Dr. W. C. C. Stirling, of Weaver, Texas, says
in the Atlanta Med. and Surg. Journal.^ April,
1889, that hemorrhagic malarial fever is
quite common in Texas, on the creeks and
rivers. . . . Drs. J.ouis and J.ynch, of
Carroll’s Prairie, Texas, assert that quinine
sometimes produces the hemorrhage. While
admitting that they are old physicians and
have treated a great many cases, the author
does not agree with them.’
Stirling (1889).
San Jacinto
I (1890)
Dock (1894).
Tyler^ St. Louis.^ South-
I (1894)
Woldert (1895).
western Railway Hospital
I (1895)
Woldert (1896).
474
Texas — continued.
Locality and Date
Cases
Authority
St, LouiSf South-western
‘ Since the year ending June 30, 1893, there
Woldert (1898).
Railway Hospital of Tyler
were five cases of malarial hemoglobinuria
admitted to the wards.’
Galveston ...
‘ A case of pernicious malarial fever of the
hematuric variety occurring in my service
last summer.’
West (1904).
Texas and Louisiana
‘ Accordingly, 2,000 blanks for report of cases
were mailed to the physicians of Southern
and Eastern Texas and Louisiana, selecting
localities where it was presumed the disease
most prevailed. Of those requested, 8 1
replied ; 40 of whom could not report cases,
while 41 reported 173 cases, to which I added
29 cases of my own, making a total of 202
- cases reported by 42 observers.’
Shropshire (1903).
Toaktim ...
Tyler
24 (1902-9)
Woldert (1912).
Colorado and Brazos
‘ In this view of the action of sulphate of.
Smith (1900).
1
Bottoms ...
quinine, I am sustained by most if not all the
physicians of my section of the country— viz.,
the Colorado and Brazos Bottoms (Texas).
It would be difficult to induce one of them to
administer quinine in malarial haematuria,
even after the haemorrhage has been
checked, for fear of reproducing it.’
Columbus
‘ Dr. John H. Bowers, of Columbus, Texas. . . .
stated to me that in his long experience,
extending considerably more than half-a-
century, he had never seen a case of malarial
haematuria in which sulphate of quinine had
been administered but what the patient died,
and that he did not recollect one in which it
was withheld but that the patient recovered.
Richmond ...
The testimony of Dr. Gibson and
Dr. Moore .... of Richmond, Texas, was
to the same effect, as also was that of the late
fV barton j
Dr. Gerard Alexander, of Wharton, Texas.’
Virginia.
Locality and Date
Cases
Authority
Richmond
i
‘ Many competent observers believe that in this
fever, especially in the graver cases , . . a
disintegration or solution of the blood discs
takes place, whereby the haematin is set free
in the circulation ; it then finds an outlet
through the kidneys. . . . Nitric acid failed
to reveal its (bilp) presence in the specimens
(of urine) examined by him.’ (p. 31 1.)
Joynes (1877).
475
Virginia — continued.
Locality and Date
^ Cases
Authority
Norfolk
.. ‘ The disease is known in this state as “ yellow
chills ” or haemorrhagic malarial fever, in
North Carolina as Roanoke yellow fever, and
! in Alabama, as the yellow disease, and is of
1 especial interest on account of its recent
j origin, rapid results, and high rate of
mortality. . . . The disease, on its first
! appearance in Roanoke Valley, was at first
1 supposed to be yellow fever and when, after-
ward, it was discovered to have a separate and
1 distinct individuality, the term Roanoke
was prefixed, to distinguish it from the true
yellow fever.’
(How m.iny cases observed not stated.)
Field (1899).
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480
ENDEMIC AREAS OF MALARIA
481
AMERICA
ACANTHOCEPHALA FROM NORTHERN
INDIA
I.— A NEW GENUS ACANTHOSENTIS FROM A
CALCUTTA FISH
BY
S. C. VERMA
LECTURER IN ZOOLOGY
AND
M. N. DATTA
RESEARCH SCHOLAR
{University of Allahabad, Allahabad, India)
Received for publication 3 May, 1929
Plates X and XI
Concerning the Acanthocephalous parasites of India very little
is so far known, but lack of published records is no indication of
scarcity of these parasites in our fauna. Within recent years some
of them have been recorded and described from India and Burmah.
Chandler (1925) was the first to bring to our notice a new species of
Centrorhynchus from Calcutta. He was followed by Subramanian
(1927 a, b, c), who dealt with a number of Burmese forms, and
Thapar (1927) who created a new genus for a worm obtained by
him from a Cyprinid fish at Lucknow. One of us (Datta, 1928) has
also published an account of a new species, Echinorhynchus robusUis,
from the common crows of Allahabad.
In the course of our parasitic survey we have collected a number
of interesting Acanthocephala from diiferent groups of hosts, and
the present paper is the first of a series dealing with them. The initial
study was restricted to fish species and two preliminary abstracts
were submitted to the Indian Science Congress held in Calcutta,
in January, 1928. One of these forms the subject of this com-
munication and the other is being prepared for the press.
ACANTHOSENTIS n.g.
Diagnosis, Acanthocephala of small size, parasitic as adults
in the alimentary canals of fishes. Proboscis short, cylindrical to
globular, armed with three circles, each composed of six single-
rooted hooks. Receptacle of proboscis cyhndrical, with a single
483
muscular waH. Body bearing 20 to 31 rings of close-set spines with
a basal plate, on anterior two-fifths of its length ; anterior circles
crowded, posterior gradually becoming more widely separated. No
spines behind middle of body. Retraction of proboscis followed or
accompanied by drawing in of anterior body. Subcuticula with
branched and oval nuclei. Central nerve ganglion near base of
proboscis sheath. Lemnisci slender, cylindrical, longer than the
proboscis receptacle. Genital organs of male in posterior half of
body cavity ; of female in posterior fourth or fifth. Testes ovoidal
or ellipsoidal, contiguous, followed immediately by a rounded
prostatic fnass of syncitial nature, with from six to eight large
nuclei. Ovary seen in very young specimens, as a small oval,
near base of proboscis sheath. Uterus with six to eight short
diverticula at commencement ; vagina narrow with two glands.
Embryos elongated, enveloped with three concentric membranes.
ACANTHOSENTIS ANTSPINUS n.sp.
Description. The small siluroid fish Aoria (Macrones) gnlio
Gunther (= Pimelodus gnlio Ham. Buch), found in abundance in
the fish markets of Calcutta from April to October and, in lesser
numbers, throughout the year, was heavily infected with this worm.
Of 90 to 100 fishes dissected during the months of May, June, and
July, 1927, and of about half as many examined in October, the
same year, nearly 80 per cent, harboured this parasite in the intestine.
The number in each host varies from ^ few to nearly one hundred.
They generally abound in duodenum and small intestine, but are
also often met with in stomach and large intestine. As usual they
are firmly attached to the intestinal wall ; but in some cases they
were observed floating freely in the lumen of the gut. On removal
to salt solution, these Acanthocephalans gradually straighten
out and perform slow movements by contraction and expansion
of the body, but appear incapable of moving in a definite direction
even for a short distance. Their internal anatomy can be studied
in hfe under pressure of a slide as the cuticle and body-wall are
fairly transparent. The specimens are best fixed expanded after
having been left overnight in normal salt solution, in cold storage.
Flattened unstained mounts show the details of the spines and the
internal musculature better than stained preparations.
48s
The colour of the worms is white, semi-transparent, but the
larger females have a brownish appearance owing to large numbers
of brown eggs within them.
The proboscis is short, cylindrical to globular, and is studded
with strong recurved hooks of the shape and dimensions given in
Text-fig. I and Table I. They are arranged in three circles of six
hooks each. Each hook is provided with a stout undivided root
Text-Fig. I. Acanthosmtis antspinusy Details of proboscis hooks : A . — Of basal circle;
B . — Of middle circle ; C . — Of terminal circle.
Table I.
Size of proboscis hooks in terms of /j,
Length of
free portion
Breadth of
free portion
Length of
root
Breadth of
root
Terminal circle ...
72*0
i6-6
42-0
13-0
Middle circle
54*0
36*0
12-0
Basal circle
48-0
12-0
25-0
11*0
486
firmly implanted in the proboscis wall and bears an inconspicuous
knob^like projection, at the anterior angle, near the commence-
ment of the free portion.
The neck is completely wanting, although a faint depression
marks the junction of the proboscis and the body proper.
The individuals vary in dimensions according to age, but average
specimens, during life, measure in mm. as follows : —
1
Length
Breadth
Males ...
i*o-i*25 mm.
0*25 0-2 mrn.
Females
Z‘o-yo nim.
o'jy-i'o mm.
The males, as a rule, are more slender and smaller than the
females of the same age and the largest of them, hardly exceed
2 mm, in length, whereas the largest females attain a length of
6 mm. or even slightly more. In Tables II and III are given relative
measurements of male and female specimens, of different ages,
respectively. The body is usually thickest about the middle, but in
some individuals, in which the anterior end is drawn in, the broadest
part is the anterior extremity [PI. X, fig. 8 and Text-fig. 2, c.]. The
anterior two-fifths of the body are covered with 20 to 31 circular
rows of minute, pointed spines with flat scaly bases or platelets
having an irregular margin [PI. X, fig. 3] as in Quadrigyrus torqualus
(Ortlepp, 1924). Of these a few of the anterior and posterior circles
have a smaller number of spines, but the middle ones carry 80 to
100 spines in each ring. In some of the older worms the spines
towards the ventral surface, in the last three to six rows, appeared
to have dropped. The genital pore is subterminal and lies in
a depression directed postero-ventrally.
A thin cuticle forms the external covering of the body-wall.
Underneath it lies the thick hypodermis or subcuticula. The
latter is traversed by a system of narrow canals forming the lacunar
system of transverse vessels (seen clearly only in living specimens
or in preparations of the body-wall) irregularly anastomising with
one another and connected with a pair of indistinct longitudinal
canals. A few large oval nuclei [PL X, fig, 5, o.n.] are clearly
487
discernible, in some preparations, situated laterally behind the
proboscis sheath : they may be present elsewhere also [PL XI,
fig. 12, o.w.]. There also occur in the subcuticula giant nuclei
of the type described by Van Cleave (1921) in the genus Quadrigyrus.
In whole mounts they are easily seen in two or three places along
the dorsal and ventral sides of the animal arranged either singly
(anteriorly) or in groups of three or more (posteriorly) [PL XI,
figs. 10, 12 and 13, b.n,]. On examining stained preparations of
portions of body-wall similar but less prominent, and more branched,
nuclei are met with in other places as well. We concur fully with
Van Cleave (1928) in bis interpretation of their nuclear nature,
and agree with him that the doubt expressed by Baylis (1927) is
unfounded. Internally to the hypodermis lies the narrow layer of
longitudinal muscles followed by a layer of circular muscle fibres.
The retraction of the proboscis (with or without inversion) and
of its sheath inwards into the body-cavity is often accompanied
or followed by a drawing in of the anterior end of the worm. The
in-drawn body-wall forms a characteristic tubular structure, with
a funnel-like opening, hanging in the body-cavity. This peculiarity
causes an interesting disposition of the muscles of the interior of the
animal, which was studied by observing the movements of living
acanthocephala under pressure of a glass slide. The drawing in of
the front part is brought about by means of a double set of retractor
muscles [Text-fig, 2, 4 and 5] which spread out posteriorly, in fan-
shaped manner, dividing the body cavity into three portions —
a dorsal, a ventral, and a median — separated from one another
only incompletely [PL XI, fig. 15, r.b.]. Of the two sets of retractors
the dorsal is more developed than the ventral and extends further
posteriorly. The eversion of the drawn end is effected partly by
the pressure exerted by the outer body-wall, partly by the relaxation
of the retractors and partly by a protractor muscle [Text-fig. 2, b, 3].
The proboscis is hollow and retractile ; it can be withdrawn
into its sheath or may remain outside it in the tubular indrawn
body-portion. At first it passes medially, without inversion ; but
in the fully retracted state, it gets inverted and is drawn, along with
its receptacle, towards the dorsal side of the body-wall [Text-
fig. 2, c]. The sheath of the proboscis has a single muscular wall
with transverse muscle fibres strongly developed and is nearly
488
one and a half times longer than the proboscis. The invertors of
the latter fill the interior of the sheath and are attached to its
anterior tip [PI. X, fig. i, rp, and Text-fig. 2, c, 6 ]. In addition to
these muscles confined within the receptacle, there pass out of its
wall posteriorly two narrow but distinct retractors which run into
the body-wall of the animal about the middle of its length. These
draw the sheath into the interior of the body-cavity. The protrusion
of the proboscis receptacle is the combined effect of the
Text-Fig. 2. Camera lucida sketches of pressed specimens showing various stages in the retraction
of the proboscis, its sheath and body end ; i and 2. — ^Protractors and retractors of proboscis sheath
respectively; 3. — Protractor of body end drawn in; 4 and 5. — Its retractors; 6. — Invertor of
proboscis.
relaxation of its retractors, the pressure of the body-wall of the
worm and the contraction of two protractor muscles [Text-fig.
2, a, i] which, arising from its hinder border, appear to run forwards
on the side of the sheath opposite to that to which it is drawn in,
namely towards the ventro-anterior end of the body.
The central nervous system consists of a single ganglion situated
within the muscular layer of the proboscis sac near the posterior
end of it. In some preparations two main trunks, the retinaculi,
are clearly seen arising from the nerve ceU. After passing out of the
489
sheath they take an undulating forward course before turning
backwards and becoming gradually indistinct.
The lemnisci are as usual two and slightly longer than the
proboscis sac. Each is provided with a single large nucleus placed
posteriorly.
The male genitalia consists of a pair of testes, vasa efferentia,
vas deferens, seminal vesicle, prostatic mass, penis, and bursa.
The two ellipsoidal or ovoidal testes, which are nearly equal in size
in extremely young males, are unequal in maturing as well as adult
individuals (for relative measurements see Table II). They lie
closely apposed to each other just behind the middle of the body
in the median line. An efferent duct arises from each and runs
backwards before joining its fellow to form the vas deferens, at the
commencement of which lies the globular seminal vesicle. The
vas deferens is a fair>sized tube full of sperms in mature males.
In some mounted specimens and in longitudinal sections the anterior
portion of the vas deferens appears saccular and packed full of
sperms. After a short, more or less straight, course backwards it
narrows and terminates in a .small muscular cone, the penis. The
prostatic gland consists of a rounded, syncitial mass containing
six to eight nuclei. It lies in close proximity of the hinder testis,
partly overlapping the seminal vesicle. It communicates with
a wide tube, the prostatic duct, lying alongside the vas deferens
and opening into the base of the penis by a narrow opening. The
penis projects into the cavity of the bursa, which is a bell-shaped
cuticular structure with a frilled margin and a pair of sacs. The
whole genitalia is covered by a thin membrane of connective tissue
and is connected through the genital ligament with the base of the
proboscis receptacle.
The female genitalia consists of ovary, bell, uterus, ovejector,
vagina, and vaginal glands. The ovary is visible as a tiny oval,
just behind the proboscis sac, in preparations of very small females.
At the termination of the post-larval stage it breaks up into packets
of cells and hence cannot be seen in toto mounts of mature females.
The ovarian packets of cells increase in number and size and, after
rupturing the walls of the genital ligament, escape into the body-
cavity in which they float about. Each of these egg masses is
enveloped by a thin membrane and contains ova in various stages
490
Tabix II.
Measurements of flattened, preserved male specimens.
No. of specimen
(large, adult)
2
(medium)
.3
(small, immature)
mm.
mm.
mm.
Total length of individual ...
2-4
17
0-8
Breadth —
At anterior end ...
038
0-21
o-o8
In middle of body (maximum) ...
0*67
0*34
o*i8
At posterior end ...
0*29
0-17
o*o8
Proboscis —
Length
0*17
q
6
0*04
Breadth ...
o‘o<;
0-04
0*04
Proboscis sheath —
Length
0*38
0-25
0*17
Breadth
0-13
0-07
0*04
Lemnlscl —
Length
0*04
0*34
0*17
Breadth
(straight)
0*07
(curved) '
0-05
(contracted)
0*04
Indrawn body end - -
Length
0*34
—
Breadth ...
0.08
—
—
Total length of genitalia ...
>'7. ..
0-63
0-38
Testes —
Anterior, length ...
0-47
(excluding bursa)
0-25
0‘o8
breadth
0*3
013
o*o6
Posterior, length ...
0*34
0*17
o*o6
breadth
0-32
015
0*05
Prostatic mass —
Length ....
017
0*07
0-025
Breadth. ...
0*21
o*o8
0-042
Seminal vesicle—
Length
0-13
o-i
(developing)
indistinct
Breadth ...
0*19
0-8
—
Bursa —
Length
' 0*21
0‘22
0*04
Breadth ... ...
o**3
(indistinct)
0-04
491
of development. When the ova are fully developed they break
away from the egg mass and fill the entire body. The fertilisation
is, as usual, internal and the embryo formation commences while
the egg is still within the body of the mother. The fertilised eggs
are characterised by the presence of three concentric enveloping
membranes round the embryo which bears a tuft of spines towards
the broader end. The eggs are elongated [PI. X, fig. 9] when ready
to be laid and measure 26/i by 8 fi. They are brownish in colour.
The bell, or uterine bell as it is sometimes called, is a triangular
funnel-like apparatus with a wide opening into the body-cavity.
It is attached to the base of the proboscis sheath by means of the
genital ligament [PI. XI, fig. 10, gl.] which keeps it in position.
At the posterior end of the bell, leading into the uterus, are given
out a number of diverticula (six to eight) which allow only properly
mature eggs to pass into the uterus. The less mature ones arc
returned into the body-cavity through a minute dorsal opening for
further development. The uterus [PI. XI, fig. ii, uf.] has thick
flabby walls containing nucleated, flask-shaped glands. The uterus
leads into the vagina through a muscular bulb, the ovejector, which
appears to control the passage of eggs into the narrow vagina. The
latter is long and the eggs generally pass through it in single file.
The vagina terminates in the genital opening which lies at the
base of a depression at the po.stero-ventral extremity of the worm.
Outside the vaginal wall lie two single-nucleated, club-shaped
glands which communicate with the vagina by a common pore
close to its external aperture. They probably secrete a fluid which
lubricates the genital opening.
Systematic position of Acanthosentis n.g. : — So far only eight
genera of adult Acanthocephala from fishes are known, in which
both the proboscis as well as the bod}^ surfaces are armed. The
present genus, which differs from them all, as will appear from the
comparative Table IV, is the ninth. The first four of the genera
mentioned in the above Table, on account of their long proboscis
with numerous hooks, double-walled -proboscis sheath and several
prostatic gland cells — not forming a single S3mcitial mass — stand
apart from the last five which agree together in possessing a short
proboscis with a small nuniber of hooks arranged in three or four
rows, single walled proboscis receptacle and a syncitial prostatic
492
ta*u m.
Measurements of flattened, preserved female specimens*
No. of specimen
(large, mature)
2
(medium)
(small, immature)
Total length of individual
4-5
(proboscis everted)
3 *S
(proboscis partly
indrawn)
0*85
(proboscis inverted)
Breadth —
At anterior end
0*6
0*9
0*2
In middle of body (maximum) ...
i*i
1-2
0-25
At posterior end
0*4
0*5
o*o8
Proboscis —
Length ...
0*2 5
0*13
(just near)
O'03
(in sheath)
Breadth
o*t5
o*t6
0-04
Proboscis sheath —
Length
0*4
(near extremity)
0*6
(in middle line)
0*2
(lateral)
Breadth
o*i8
O'is
0'06
Lemnisci —
1
Length
0-9
twisted
o*r4
Breadth
O' I
__
0*03
Indrawn body end —
Length
—
07
0-15
Breadth
—
0-3
o*o6
Total length of genitalia
0-9
07
0-25
Bell--
Length
0-3
0*25
0-05
Breadth
0*25
0*2
0*04
Uterus —
Length
0*25
0*28
0*03
Breadth
N^agina— •
0'05
0*05
0*01
Length'
0-3
0*28
0*12
Breadth
9*05
0*05
0*Qt
Vaginal gland
Length
o'ls
0*08
(contracted)
indistinct
Breadth
o*o6
0*05
493
mass with a few large nuclei, except Acanihogyrus in which it is
double with two or more nuclei in each. The new genus, included
in the latter group, is readily distinguished from the others by the
number and arrangement of its proboscis hooks, by the structure
of the prostate, by the structure and disposition of the body spines and
by the character of its subcuticular nuclei.
Southwell and Macfie (1925) placed the first three genera,
namely, Rhadinorhynchus, Telosentis, and Serrasentis in the family
Rhadinorhynchidae, sub-order Echinorhynchidea. For the fourth,
T egorhynchus , together with some others, they created a new family
Corynosomidae under the same sub-order as Rhadinorhynchidae.
Travassos (1926) has placed all the four together in the family
Rhadinorhynchidae with two others : his system of classification
does not erect orders and sub-orders, groups higher than the family.
Thapar (1927) has taken a new line by disregarding the basis of
previous classifications. He suggests the presence or absence of
spines on the body and proboscis, and the single or double root of
proboscis hooks as characters showing natural affinities. The
first of the above two characters have been incorporated in the
previous systems referred to above, though in a different way ; but
Thapar had not seen Travassos’s (1926) publication as there is no
reference to it in his paper. The other character is a new suggestion
worthy of consideration by future workers on the group. In the
tentative scheme of classification proposed by this author the first
six genera of Table IV are inserted in his new family Acantliogyridae,
which includes a number of other genera as well, all characterised by
possessing single-rooted proboscis hooks. The family is placed in
his new order Acanthogyridea (class Acanthocephala) , all members
of which have cuticular spines on the body. According to this
criterion the last three genera also fall in the same category, though
Van Cleave (1928), apparently unaware of Thapar's work, has
erected a new family, Pallisentidae, for his two genera Pallisentis
and Neosentis, Thus Thapar has massed together forms differing
from one another in important details of anatomy such as the size
of proboscis, number and arrangement of hooks on it, the character
of the wall of its receptacle, the location of the central nervous
system and the nature of the prostate gland.
It is not desirable on our part to suggest radical changes in the
494
existing systems (imperfect though they may appear) based on the
direct study, however careful, of a few genera only. We therefore
hope to revert to this subject later, after our more extensive survey
of Indian types is completed, for it may throw illuminating light
on the points at issue. With our present knowledge of the group,
we consider it premature to give an isolated character (as the single
or double root of hooks on the proboscis) predominance over
a combination of no less important characteristics, in making it the
basis of division into families. Moreover there exist types, like
Acanthocephalus anguillae (Miill) [Liihe, 1911, page 14], in which
the proboscis hooks have neither single nor double root, but are
distinctly three-rooted (tri-radiate). In quite a number of other
forms the roots show great variation in passing from one end or side
of the proboscis to the other. A reptilian worm obtained by one
of us (Verma), which will be described later, has the anterior hooks
very complicated but the posterior ones extremely simple.
For the present, therefore, adopting Travassos’s (1926) classifica-
tion, we propose coupling our genus Acanthosentis with Quadrigyrus,
with which it shows the closest affinity, into the sub-family
Quadrigyrinae (Van Cleave, 1920) of the family Neoechinorhynchidae
(Travassos, 1917). According also to Southwell and Macfie's scheme
it will fall in with the same genus, but in the family Quadrigyridae
of the sub-order Neoechinorhynchidae, order Acanthocephala. The
family of Travassos is nearly equivalent to the sub-order of Southwell
and Macfie, and his sub-family to the latter authors* family. Further,
to avoid unnecessary multiplication of families for closely related
forms, it would be better to include the genera Acanthogyms ,
Pallisentis and Neosentis in the same family or sub-family with the
above two genera, and to allow the iamilies Acanthogyridae and
Pallisentidae to merge into Quadrigyridae with the following
emended definition : —
Acanthocephala of small to medium size. Proboscis short,
with few rows of simple rooted hooks. Body arnied with spines
arranged in one or two series of complete or incomplete rings or
scattered or both. Receptacle of proboscis with single muscular
wall. Brain at or near base of receptacle. Prostate a syncitial
mass, rarely double, with few large nuclei. Nuclei of subcuticula
oval or branched or both. Parasitic in fishes.
495
Table IV.
Diagnostic characters of piscine genera of Acantliocephala, possessing armed proboscis and body.
Name of genus
Proboscis
and
its hooks
Wall of
proboscis
receptacle
Location
of brain in
receptacle
Prostate
gland
Body spines
Sub-
cuticular
nuclei
Rhadinorbyttchus ...
Luhe, 1911
Long : hooks numerous,
ventral stronger than
dorsal.
Double.
Near middle
Not a single syncl-
tial mass.
Scattered, powerful ;
only on anterior part.
Small and num-
Tdosenih
V^an Cleave, 1920
do.
do.
do.
do.
Scattered ; on pos-
terior extremity only.
, crous, or few
large finely
dendritic.
Serramtis
Van Cleave, 1923
do.
do.
do.
do.
A collar anteriorly,
followed by 18 to 23
ventral rows.
Tegorhynchus
Van Cleave, 1920
Long ; hooks numerous,
but symmetrical.
do.
At anterior
end.
do.
(several cells,
elongated)
An uninterrupted man-
tle from anterior end
backwards ; none on
posterior end.
Ouudrigyrm
Van Cleave, 1921 '
!
Short : 4 circles of 5
each.
Single.
Near base.
Compact, synci-
1 tial; nuclei few,
1 large.
In four circles ; on
anterior surface.
'I'wo ovoid, ante-
rior ; few
branched scat-
tered.
Acanthogyrus ...j
I'hapar, 1927 '
Short : 3 circles of 8
each.
do. j
1
j
At base.
! Spherical double
1 mass ; nuclei two
or more in each.
19-20 circles anteriorly
followed by 20-21
paired lateral ones,
to posterior end.
Pallismis
Van Cleave, 1928 j
1
Short : 4 circles of 6
each.
do. j
i
Near base.
\'cry long, synci-
tial ; nuclei few,
large.
6-9 rings anteriorly ;
20-40 rings further
back.
N mentis '
Van Cleave, 1928
Short : 4 circles of 8
each.
i
i
1
1
do. 1
'
At posterior
end.
!
Long, syncltial ;
1 nuclei 16, large.
5-6 circles anteriorly ;
6-8 further back ;
scattered ones on
anterior third.
Acanlhoscnth
n.g., 1928
1 Short : 3 circles of 6
each.
do.
1
1 Near base.
Compact, syncl-
tiai J nuclei 6-8,
large.
20-31 rings on anterior
two-fifths.
Lew oval and
branches.
496
REFERENCES
Baylis, H. a. (1927)- Some Parasitic Worms from Arapaima gigas (Tclcostcan fish) with
a description of Pbilometra senticosa n.sp. (Filaroidca). Parasim^^ IS, 35-47-
Chandler, A, C. (1925). The Helminth Parasites of Cats in Calcutta and the Relation of Cats
to Human Helminthic Infections. Ind. Jl. Med, Res., 13 , 222-223.
Daita, M. N. (1928). On Ecbinorbynchus robustus, n.sp. from common crows, Corvus corax and
Corvus splendens of Allahabad. Allahabad Untv. Stud., 4 , 41-61.
Lube, M. (1911). Die Slisswasserfauna Deutschlands. Heft XVI, Acanthocepbalen, Jena, pp. 14
and 44-46.
Ortlepp, R. J. (1924). On a collection of helminths from Dutch Guinea. Helminthol., 2 , 15-40-
Southwell, T., and Macfie, J. W. S. (1925). On a Collection of Acanthocephala in the Liverpool
School of Tropical Medicine. Ann. “Trop. Med. & Parasitol., 19 , 141-184.
Stiles, C. W., and Hassall, A. (1920). Index Catalogue of Medical and Veterinary Zoology.
Subject : Roundworms. Bull. No. 1 14, Hyg. Lab., Washington.
Subramanian, K. (1927). On a new genus of Acanthocephala from Rangoon. Ann. Mag. Nat-
Hist., Ser. 9, 19 , 275-279.
(19-7)- Oil small collection of Acanthocephala from Rangoon. Ann. Mag. Nat. Hist.,
Ser. 9, 19 , 645-650.
(1927). Note on the larva of Centrorhynebus aluconis (Muller 1780) (Acanthocephala)
found in Rangoon toads, yi. Burma Res. Soc., 16 , 211-212.
'i'liAPAK, G. S. (1927). On Acantho^yrus, n.g., from the Intestine of the Indian Fish Labco robita,
with a Note on the Classification of the Acanthocephala. yi. Helminthol., 5 , 109- 120.
I'ravassos, 1-. (1926). Rcvis3o dos Acanthoccphalos brasileiros. Parte II. Familia Echino-
rhynchidae Hamann, 1892. Mem. Inst. Oswaldo Cruz., 19 , 31-125.
Van Cleave, H. J. (1921). Two new genera and species of Acanthocephalous worms from
V'cnezuclan fishes. Proc. U.S. Nat. Mus., 58, 456-466.
(1923). A Key to Genera of Acanthocephala. Trans. Amer. Micros. Soc., 42 , 184-191.
(1928). Nuclei of the Subcuticula in the Acanthocephala. Zeit. fur Zellfor. Micros.
Anat., 7 , 109-113.
- ■ (1928), Acanthocephala from China. I. — New species and New Genera from Chinese
Fishes. Parasitol., 20 , 1-9.
Plate X
EXPLANATION OF PLATE X
Fig. I. Lateral view of male specimen pressed and mounted.
Fig. 2. Proboscis showing arrangement and number of hooks.
Fig. 3. Some body spines, highly magnified.
Fig. 4. Photomicrograph of transverse section through anterior
region of a male worm.
Fig. 5. Young male with developing prostate.
Fig. 6. Male genitalia,, after dissection.
Fig. 7. Vertical section of adult male passing through the repro-
ductive organs.
Fig. 8. Magnified view of three eggs.
All figures, with the exception of Number 4, were drawn with
Abbe’s Camera Lucida.
REFERENCES TO LETTERING
h.
~ bursa.
P-
=
proboscis.
b.n.
— branched nucleus.
p.d.
=
prostatic duct.
b.s.
— body spines.
pe.
=
penis.
c.
— cuticle.
P-g'
—
prostatic gland or mass.
c.m.
~ circular muscle fibres.
p.h.
_=
proboscis hooks.
— dorsal retractor of proboscis sheath.
p,s.
proboscis sheath or receptacle.
I'.Vl,
■- egg mass.
r.b.
retractor muscle of body end.
A'-/-
— genital ligament.
r.p.
=
retractor or invertor muscle of
S-P-
— genital pore.
proboscis.
h.
— hypodermis or subcuticula.
s.m.
spongy muscles.
1.
— lem nisei.
s.v.
seminal vesicle.
l.m.
= longitudinal muscle fibres.
u
=
testes.
n.
~ nucleus.
u.
uterus.
n.f.
= nerve fibre or retinacutuin.
u.b.
=
uterine bell.
n.g.
= nerve ganglion.
u.d.
~
uterine diverticula.
0 .
= ovary.
V,
=
vagina.
oe.
= ovejector.
V.d.
=
vas deferens.
o,m.
~ ova with enveloping membranes.
v.c.
vas efferens.
Q.n.
= oval nucleus.
v.g.
=
vaginal gland.
ov.
= eggs or fertilised ova.
v.r.p.s.
=
ventral retractor of proboscis sheath.
Plate XI
EXPLANATION OF PLATE XI
P'ig. 10. Lateral view of adult female, pressed and mounted.
Fig. II. Female genitalia after dissection ; much magnified.
Fig. 12. Part of body-wall in toto mount showing branched and oval
nuclei.
Fig. 13. Transverse section of body-wall through a branched
nucleus.
Figs. 14-16. Photomicrographs of transverse sections of a female
specimen passing through the proboscis sheath, the
middle of the body, and the uterus respectively.
Fig. 17. Egg masses, entire and split up, showing developed ova.
All figures, except Numbers 14 to 16, were drawn with Abbe’s
Camera Lucida.
For references to lettering see explanation of Plate X.
STUDIES IN CHEMOTHERAPY*
I. A METHOD FOR MAINTAINING PATHOGENIC
TRYPANOSOMES ALIVE IN VITRO AT 37^0.
FOR 24 HOURS
BY
WARRINGTON YORKE
A. R. D. ADAMS
AND
F. MURGATROYI)
[Received for publication, 7 October, 1929)
As a preliminary step in an investigation designed with the
object of obtaining some insight into the mechanism of the action
of certain arsenical preparations in experimental trypanosomiasis,
it appeared desirable to examine the action of the drugs in question
on the parasites in vitro.
Unfortunately, all attempts to culture the pathogenic trypano-
somes have hitherto been unsuccessful, and yet it is at once obvious
that before we can proceed with an investigation of this nature,
some method must be discovered whereby the trypanosomes can be
maintained alive in vitro for such a length of time as will enable
one to judge definitely whether the addition of the drugs to the
medium has, or has not, any trypanocidal effect. During the past
thirty years many workers have interested themselves in the question
of the action of drugs on trypanosomes in vitro, and the number of
papers relating to the subject is very considerable. It is,
consequently, not surprising that the literature dealing with the
maintenance of trypanosomes in vitro is also voluminous. We do
not propose to refer to the great majority of these papers, beyond
observing that they reveal many contradictory statements and
• This work was supported by a grant from the Chemotherapy Committee of the Medical
Kescttrch Council.
502
anomalies and, generally speaking, are of little value for the object
we have in view, as they contain no precise quantitative information.
There seems to be, however, a more or less general agreement that a
medium consisting wholly, or partly, of serum maintains try-
panosomes better than physiological saline and the various modifica-
tions of Ringer's solution ; and that the parasites survive longer
at laboratory temperature than at 37° C. Terry (1911 and 1915),
who examined the trypanocidal action of certain drugs in vitro,
concluded that all the sera he used — rabbit, ox, horse, goat, sheep,
pig, chicken, rat and mouse — preserved the motility and the
morphology of Trypanosoma hrucei better and longer than did salt
solution and various modifications of Ringer's solution. He states
that the serum should not be diluted more than two to four times,
that undiluted serum is the best, and that the parasites are better
preserved at room temperature than in the ice-box ; he adds that
the infectivity of trypanosomes suspended in ox serum at room
temperature was maintained for at least eight days. Apparently, no
observations were made at 37"^ C. Rothermundt and Dale (1912),
in an interesting paper on the action of atoxyl in vitro and in the
animal body, likewise discuss the problem of maintaining trypano-
somes in vitro. They found that whereas trypanosomes suspended
in physiological saline died within a period of two hours at 37° C.,
and lived for only two to two and a half hours at laboratory
temperature (22'^ C.), their survival was prolonged to a period
varying from two to five hours at 37° C., and from eight to twenty-
four hours at 22° C., when the parasites were suspended in
defibrinated guinea-pig blood. They subsequently discovered that
guinea-pig serum was distinctly superior to defibrinated blood, and
that in this medium the parasites remained alive at 37° C. for at
least five hours. Kligler and Weitzman (1925) studied the action
of Bayer 205 in vitro, and during their work found that T, evansi
could be kept alive in guinea-pig serum diluted with saline for at
least twenty-four hours at 25° C. ; no details are given beyond the
fact that certain of the parasites were, at the end of this period,
actively motile and infective ; apparently no observations were made
37^ C. Papamarku (1927) made an extensive study of the
action of certain drugs on trypanosomes and spirochaetes in vitro.
He employed deactivated rabbit serum as a medium for suspending
the parasites ; this 'was inoculated by the addition of a drop of
infected blood, and the medium was then covered with a layer of
liquid paraffin. Under these conditions, Papamarku found that the
motility of the trypanosomes was preserved for at least forty-eight
hours at room temperature ; here again, however, there is no record
of observations made at 37 C.
Preliminary experiments soon convinced us of the truth of
the main conclusions reached by previous workers ; namely, that
when suspended in serum the trypanosomes survive much longer
than in physiological saline or in various modifications of Ringer’s
solution, and that the period of survival is considerably greater at
laboratory temperatures than at 37° C. We were, however, early
impressed by a fact which, although it had possibly not escaped
the notice of those who had previously investigated the subject,
yet is certainly not referred to by them. In many of our experiments
a progressive diminution in the number of trypanosomes set in shortly
after the commencement of the experiment ; careful microscopic
examination showed that whilst many of the parasites were actively
motile and of normal appearance, others were sluggish or even
motionless, and some were clearly in various stages of disintegration.
This, of course, means that under the same conditions of experiment
certain individuals died relatively quickly and then disintegrated
and finally became unrecognisable, whilst others remained actively
motile and apparently in good condition for much longer periods.
It should further be mentioned that in our preliminary work the
results obtained were far from constant ; for example, in some
experiments the trypanosomes suspended in rabbit serum died
much more quickly than was the case in other experiments in which
the same medium was employed.
Considerations of this nature led us, therefore, to re-investigatc
the whole subject, with the object of obtaining, so far as was possible,
precise information having a quantitative value, and of devising a
method whereby trypanosomes could be kept alive, without serious
diminution in the original number introduced into the medium, for a
period of at least twenty-four hours at 37"’ C. Notwithstanding the
fact that it is generally recognised that it is much easier to keep
trypanosomes alive in vitro at laboratory temperature than at
37° C,, the ultimate object we had in view — the investigation of the
504
trypanocidal action of drugs in vivo — compelled us to concentrate
our attention on experiments conducted at 37'' C. It is a remarkable
fact that almost without exception all those who have concerned
themselves with the action of drugs on trypanosomes in vitro have
worked at comparatively low temperatures. This can only mean
a general recognition of the difficulty of keeping the parasites alive
in vitro at body temperature.
As preliminary observations appeared to confirm the conclusion
of previous workers, that serum was the best medium for
supporting trypanosomes in vitro, we decided at first to confine our
attention to this medium, and then, having ascertained under what
conditions the best results were to be obtained with it, to compare
tliose given with other media under similar conditions.
I'he trypanosomes used in these experiments were : (i) a strain
of T. eqiiiperdum, about which little is known beyond that it has been
maintained for many years in European laboratories by passage
through mice ; (ii) a strain of T. rhodesiense, which was isolated from
man in 1923, and which has since been kept in mice ; and (iii) a strain
of T, gambiense isolated from man in March, 1922, and since main-
tained in mice.
Technique. A mouse at the height of the infection, when its blood
was swarming with parasites, was killed with chloroform, and blood
obtained from the heart with aseptic precautions was diluted with
twice its volume of sterile citrated saline solution. After mixing
thoroughly, i volume of this was added to 9 volumes of rabbit
serum ; this, which we call Suspension A, was, therefore, a 30-fold
dilution of the infected blood. Suspension B was made by taking
I volume of Suspension A and adding it to 9 volumes of rabbit serum,
and Suspension C by diluting i volume of Suspension B with
9 volumes of rabbit serum. By this means various dilutions of the
infected blood in rabbit serum were obtained, viz., Suspension A, in
which the infected blood was diluted 30-fold ; Suspension B, in which
the dilution was 300-fold ; and Suspension C, in which it was
3,ooo-fold. About i*o c.c. of each of these suspensions was then
added to each of a series of sterile glass tubes, and incubated at
37° C. These tubes, which were about 7-5 mm. in bore and 7^5 cm.
in length, were made in the laboratory from ordinary stout-walled
glass tubing, and were covered by caps made from ^ass tubing of a
505
slightly larger diameter.* Samples were removed from time to time
with a sterile pipette — care being taken to mix thoroughly the
contents of the tube — and examined, microscopically, on a Thoma
Zeiss haemocytometer slide with the combination, Leitz Oc. 2, Obj. 6.
By this means, it was found that the number of trypanosomes present
in a suspension could be determined with reasonable accuracy,
provided the concentration did not exceed about 60 parasites to the
256 small squares of the haemocytometer scale, i.e., approximately
1,000 per c.mm. It was found that in the case of very heavily
infected mice, Suspension C, representing a 3,000-fold dilution of the
infected blood, gave, as a rule, a count of between 30 and 60 parasites
for the 256 squares of the haemocytometer scale.
Tablh I.
i Concentration j
I of infected j Number of living trypanosomes per 256 squares of the
Tube 1 mouse blood 1 haemocytometer scale
1
in tresn
rabbit serum
Start
2
hours
4
hours
6 9
hours hours
1 1
hours
*3
hours
^5
hours
I
I : 30
(7,000)
4-++*
57 *
2
I : 30
+++*
! ... 0*
3
I ; 300
(700)
570
1 ... 640
620
t -*
4
I : 300
648
20*
5
I ; 3,000
67
82
...
108
*88
1 7 *)
6
I : 3,000
105
'84
66
7
l ; 30,000
7
7
16
10 9
...
>4
5
8 i
1
I : 30,000
10
>3
>4
6
The figures in brackets are calculated numbers, and the large numbers (over 100), have only an
approximate value.
Indicates living trypanosomes too numerous to count ; many large agglomerations seen.
^ l.arge numbers of dead and degenerate parasites also seen.
Numerous experiments of this nature were performed with the
various strains of trypanosomes, using fresh and deactivated rabbit
serum as a medium. The results obtained were constant and are
illustrated by the typical protocol set forth in Table I.
•.The discovery of a suitable covering for the tubes proved to be a matter of some difficulty.
At first, following Papamarku, the contents of the tubes were covered with a layer of liquid paraffin 5
this was, however, found unsuitable for our purpose, as the paraffin droplets interfered with the
enutnefation of the parasites in the haemocytometer. Plasticine caps and cotton-wool plugs were
also trifd, but both had to be abandoned, as the heating of the tops of the tubes for the purpose of
sttriUzation resulted in the production of substances toxic to the trypanosomes. The smdl amount
of dust faSitig from sterlfired cotton-wool plugs also seemed to have a detrimental effect on the
trypanosomes, whidi showed a marked tendency to adhere to minute solid particles.
5o6
From the experiment recorded in this table it will be seen that
when the infected mouse blood was diluted 3,000 times, the number
of living parasites was substantially the same at the end of 24 hours
as it was at the beginning of the experiment. This does not
imply that all the individual trypanosomes originally present in the
suspension had survived during this period. As a matter of fact,
occasional dead and degenerate forms were seen throughout the
whole period. The numbers were, however, maintained by
multiplication of the parasites.
Divisional forms were seen throughout the experiment, and during
the early hours division proceeded at such a rate that it more than
balanced the loss due to death, with the result that the total number
of parasites increased substantially. As time went on, the rate of
rnultiplicE^tion either subsided, or the death rate increased, so that the
total number of parasites gradually decreased until, at the end of
24 hours, the number was about the same as at the beginning
of the experiment. This likewise applied in the cases where the
dilution of the infected blood was i : 30,000. When, however, we
turn to the observations where the dilutions were only i : 300 or
I : 30, death occurred much more rapidly. In the i : 300 dilutions,
the number of parasites remained more or less stationary for about
12 hours and then fell rapidly, so that after 24 hours only a small
fraction of the original number was still alive. In the i : 30 dilutions
death occurred with great rapidity within an hour or so large
agglomerations of sluggishly-moving parasites, many of which were
degenerating, were to be seen, and within 6 hours the great majority
were dead and degenerate.
As frequent observations of this nature indicated that the degree
of dilution of the infected blood influences to a very definite extent
the length of survival of the parasites in rabbit serum at 37° C.,
experiments were devised with the object of determining whether
it was the concentration of parasites, or that of the serum of the
infected mouse, which was the determining factor in producing
this result.
Experiment. To 0*5 c.c. of cit rated-saline was added 0*25 c.c. of the heart
blood of a mouse, taken at the height of infection with T. rhodesievse^ and from
this, 30-fold (Suspension A), 300-fold (Suspension B) and 3,000-fold (Suspension' C)
dilutions in fresh rabbit serum were made as previously described. About 2*5 c.c.
of Suspension A was centrifuged at high speed, the deposit of trypanosomes washed
507
thrice in fresh rabbit scrum, and finally fresh rabbit serum added to the washed
deposit so as to bring the volume once more up to 2*5 c.c., thus giving a concentration
of washed parasites (Suspension D) corresponding to that of the 30-fold dilution of
mouse blood. From this Suspension E and Suspension F were made, corresponding
to the 300-fold and the 3,000-fold dilutions of mouse blood. Each of the six
suspensions was divided amongst a number of tubes which were placed in a water
bath at 37® C., and to one tube of each of these was added one-twentieth of its
volume of the centrifuged serum of the infected mouse, with a view to ascertaining
whether possibly any antibodies it might contain exercised an unfavourable action
on the longevity of the trypanosomes.
The results of this experiment, which are set forth in Table II,
indicate clearly that the factor which determines the longevity of the
parasites in rabbit serum is not the concentration of the serum of
the infected mouse, but that of the parasites. That this is so is not
surprising, when one considers the enormous activity of the trypano-
somes. Very little is known of the metabolism of trypanosomes.
Experiments performed many years ago (Nauss and Yorke, 1911)
showed that the incubation, in the absence of air, of living trypano-
somes in defibrinated blood causes, if the parasites be numerous, a
total disappearance of the oxygen combined with the haemoglobin ;
the carbon dioxide is not increased in a degree corresponding to
the diminution of oxygen. There seems no reason to doubt that
the parasites absorb their protein and carbohydrate material in the
liquid state from the medium in which they are living ; and it is
quite probable that the shorter life of the parasites in the more
concentrated suspensions is due, in part at least, to the more rapid
exhaustion of the nutrient material in the medium. It is also
possible that the products of metabolism are unfavourable to the
life of the parasite, and that their more rapid accumulation in the
concentrated susf)ension of trypanosomes constitutes another of the
factors which curtail the length of life of the parasites in such
suspensions, as compared with weaker suspensions.
The work of Biot, Biot and Richard (1911), and that of Schern
(1925), and others, has shown the importance of glucose in the
metabolism of trypanosomes. In our preliminary experiments we
were impressed by the fact that serum which had been kept for some
time, and which had become contaminated by bacteria, had lost,
to a considerable extent, its power of supporting trypanosomes, even
though it had been sterilized by heating to 60® C. for half an hour on
several occasions before use. The addition of a small quantity
5o8
Table II.
Concentration
of infected
! Wood, or Number of living trypanosomes per 256 squares of the
' haemocvtometer scale
concentfft- ^
rui>e
jtlons of wash-
i ed parasites,
j in fresh
' rabbit serum
Start
Jhour
2
hours
3
hours
4
hours
5
hours
6
hours
hours
10
hours
12
hours
i
Suspension A
I :30
(4,000)
1
++++++
...
+++
...
...
3 c>*
10*
2*
2
Suspension A
...
(4,000)
...
...
...
...
50 *
...
...
...
3
Suspension A -f -A vol. of scrum
of infected mouse
(4,000)
++++++
...
+++
...
...
45 *
13*
I*
4
Suspension B
I : 300
(+00)
...
...
450
...
440
435
485
435
5
Suspension B ...
...
(400)
...
...
...
...
...
...
...
...
C
Suspension B -f A vol. of serum
of infected mouse
(400)
336
475
...
410
340
280
250
7
Suspension C
1 : 3,000
36
...
48
48
55
56
52
S
Suspension C
...
34
...
...
...
...
...
Suspension C -[ • A vol* of scrum
of infected mouse
4 ^> :
...
...
47
47
...
56
57
4 fi
lu
Suspension 1 )
1 130
(4,000)
...
'f-l-*
50*
1 10*
1*
11
Suspension 1 )
(4,000)
...
...
...
45 *
...
...
12
Suspension 1 ) 4 * A vol. of scrum
of infected mouse
...
(4,000)
...
...
4 H-I-
++
5 *
o»
13
Suspension £
I 1300
(400)
...
380
39 i
...
380
352
358
1
Suspension E
...
(400)
392
...
...
...
...
...
...
...
15 I
Suspension E + A vol* of scrum
of infected mouse
...
(400)
...
...
450
345
...
450
416
392
16
Suspension E ... !
1 : 3,000
40
...
...
39
41
...
64
50
45
n
Suspension E
...
39
...
...
...
...
...
...
....
...
18
Suspension F -f A vol* of scrum
of infected moUse ‘
...
34
...
...
40
58
52
46
53
The figures in brackets are calculated numbers, and the large numbers (over 100), have only an approximate value.
Indicates living trypanosomes too numerous to count*, many large agglomerations seen.
* Large numbers of dead and degenerate parasites also seen.
S09
(o‘i per cent.) of glucose to such a serum sufficed to restore in a large
measure its nutrient qualities. With the object of investigating
the matter further, experiments of the following nature were under-
taken.
Experiment. Blood from the heart of a mouse at the height of infection with
T. rhodesiense was diluted with an equal volume of citratcd saline, and i c.c. of the
citrated blood was then added to 9 c.c. of deactivated sheep serum. This mixture
was placed in the incubator at 37° C. and shaken from time to time. After 3 hours
it was centrifuged at high speed and the supernatant fluid, ‘Extracted serum,’
removed. The capacity to sustain trypanosomes of the ‘ Extracted serum,’ and of
the various modifications of it shown in Table HI, was examined in the manner
already described.
The data supplied in Table III demonstrate that the presence of
large numbers of trypanosomes in serum for a period of 3 hours
at 37'^ C. impairs, to a marked extent, its capacity to support trypano-
somes, and furthermore, that the addition of o-i per cent, glucose
suffices to restore its nutrient qualities. The conditions of the
experiment failed to reveal the presence in the ‘ Extracted serum '
of any substance highly toxic to the trypanosomes. If such toxic
substances had been produced in any quantity, one would have
Table 111 .
Trypanosomes per 256 squares of
the hacmocytometcr scale
1 UDC
; Start
n
hours
41
hours
7 f
hours
19
hours
I
1
Extracted scrum
76
88
94
3
0
2
Extracted scrum
1
0
3
Extracted scrum + o*i % glucose |
7 ^
78
1 08
1 06
79
4
Extracted scrum + o*i % glucose |
...
95
5
Extracted scrum 0*5 c.c. -{- normal sheep scrum 0*5 c.c. j
77
81
85
<>9
6
Extracted serum 0*5 c.c. -f- normal sheep scrum 0*5 c.c. i
77
60
7
1
Saline 0*5 c.c. -f- normal sheep serum 0*5 c.c.
71
1
74
77
7 *
8
Saline 0*5 c.c. -b normal sheep serum 0*5 c.c.
62
...
64
9
Normal sheep serum j
65
73
87
65
10
Normal sheep serum
73
...
65
expected that the mixture, consisting of equal parts of the ' Extracted
serum ' plus normal serum, would have proved less favourable as a
medium for supporting tr5q)anosomes than equal parts of physio-
logical saline plus normal serum ; such, however, was not the case.
In view of the striking results given by experiments of this kind,
we decided to ascertain whether, by chemical analysis, it was possible
to demonstrate that the suspension, in serum, of numerous trypano-
somes at 37*^ C. for various periods, resulted in a removal of glucose
from the serum.
Experiment. In each of two wide glass tubes, A and B, was placed 5 c.c. of
sheep serum which had been heated to 56° C. for 30 minutes. To one of these.
Tube B, was added lo mgm. of glucose. The heart blood of a mouse heavily infected
with T. rhodjesiense was then withdrawn into an equal volume of citrated saline, and
0*5 c.c. of th^ citrated blood was added to each of the two portions of sheep serum.
The suspensions were immediately placed in the water bath at 37° C. and agitated
at frequent intervals. It was observed that the colour of each changed within a
few minutes from bright red to dark purple, owing to the reduction-of the oxyhaemo-
globin of the mouse red cells. On shaking, the bright red colour was immediately
restored.
At the end of an hour, Suspension A no longer turned purple, and examination
showed that practically all the trypanosomes were dead ; it was then centrifuged at
liigh speed and the supernatant fluid ‘ Extracted scrum A,’ removed and set aside
for sugar estimation. Suspension B continued to turn purple and the trypanosomes
to exhibit active motility for a further period of 4J hours, when both the reduction
of the haemoglobin and the motility of the parasites ceased ; it was then centrifuged
and the supernatant fluid, ‘ Extracted serum B,’ removed.
The sugar content of the original sheep scrum and of the ‘ Extracted
sera A and B ’ was determined with the following results : —
Original sheep scrum, 50 mgm. per 100 c.c.
‘ Extracted serum A,’ less than 10 mgm. per 100 c.c.
‘ Extracted serum B,’ less than 10 mgm. per 100 c.c.
Analysis of the data supplied by this experiment conveys some
idea of the enormous consumption of sugar in the metabolism of
trypanosomes. The trypanosome suspensions consisted roughly of
5 c.c. of serum and 0*25 c.c. of infected mouse blood, i.e., the dilution
of infected blood was approximately 20-fold, and the concentration
of trypanosomes approximately 80,000 per c.mm. The quantity of
sugar in Suspension A was 2-5 mgm. and that in Suspension fe,
12*5 mgm. Apparently, therefore, the trypanosomes in 0*25 c.c. of
infected mouse blood (i.e., 400 millions) sufficed, within i hour,
to cause the disappearance of between 2 mgm. and 2*5 mgm. of sugar,
and, within 5 hours, of between 12 mgm. and 12-5 mgm* In experi-
ments of this sort, where concentrated suspensions of trypanosomes
S«I
were used, the length of life of the parasites appeared — within, of
course, certain limits — to vary directly with the amount of sugar
available.
Having ascertained that trypanosomes consumed large quantities
of sugar, and that the length of life of the parasites in concentrated
suspensions is largely determined by the amount of sugar available,
we proceeded to enquire whether any evidence could be obtained
that more prolonged sojourn of numerous trypanosomes in serum
resulted in the production of changes in the serum other than the
mere removal of glucose.
Experimf.nt. To 15 c.c. of sheep serum was added 1*5 c.c. of a mixture of
equal parts of citrated saline and the heart blood of a mouse heavily infected with
T, rhodesiense^ and the resulting suspension was immediately placed in the water-
bath at 37° C. Within a few minutes the colour was observed to have changed
from bright red to dark purple ; on shaking, the red colour immediately returned.
The suspension was shaken every few minutes during a period of 2J hours, at the
end of which time very little reduction occurred, and practically all the trypano-
somes were found to be dead and degenerate ; it was now centrifuged at high speed
and the supernatant fluid removed and divided into 3 equal volumes, the first of
which, * Extracted fluid A,’ was set aside ; and to the third, C, was added sufficient
glucose to produce a 0‘i per cent, concentration. To each of the Portions, B and C,
was then added 0*5 c.c. of the citrated heart blood of another mouse heavily infected
with T. rhodesiense, and the suspensions again placed in the water bath at 37° C.
It was observed that both suspensions speedily became dark purple ; they were
frequently shaken as before. After 30 minutes it was found that Suspension B turned
purple very slowly, whilst in Suspension C the reduction occurred with the previous
rapidity. At the end of 60 minutes, reduction had ceased in Suspension B, and
all the parasites were dead ; this suspension was then centrifuged at high speed
and the supernatant fluid removed — ‘ Extracted fluid B.’ In Suspension C,
reduction continued actively for another 2 hours ; it then became slow and finally,
after a further 30 minutes, ceased altogether, and practically all the trypanosomes
were dead. Suspension C was then centrifuged at high speed and the supernatant
fluid, ‘ Extracted fluid C ’ removed.
The sugar content of each of the three extracts and of the original sheep serum
was then estimated, with the following results : —
Original sheep serum, 51 mgm. per loo c.c.
‘ Extracted fluid A,’ less than 10 mgm. per 100 c.c.
‘ Extracted fluid B,’ less than 10 mgm. per 100 c.c.
‘ Extracted fluid C,’ less than 10 mgm. per lOO c.c.
The capacity to sustain trypanosomes of the original serum, of the three extracts,
and of the various modifications of them shown in Table IV, was examined in the
usual manner.
The results of the experiment recorded in Table IV show once
again that the primary change produced in serum by the action of
numerous trypanosomes is the loss of glucose. Serum treated in
this manner (Extract A) quickly loses its capacity to support trypano-
512
somes, and that this is mainly due to lack of glucose is seen from
the restorative action of the addition of o*i per cent, glucose. When,
however, the serum has been subjected to still more prolonged action
of the parasites (Extract B and Extract C), the addition of o*i per
cent, glucose, although it restores in very large measure the nutrient
properties of the serum, apparently fails to do so completely, with
the result that trypanosomes added to such media die more quickly
than in untreated sheep serum.
Table IV.
Tube
Number of living trypanosomes per 256 squares of the
haemocytometcr scale
Start
i
hour
I
hour
li
hours
3
hours
5
hours
7
hours
9
hours
12
hours
26
hours
1
Extract A
64
62
54
33
»9
' *7
12
12
0
2
Extract A + o' 1% glucose
...
59
74
77
94
98
21
3
Extract A 1 part, sheep serum i part ...
...
72
...
gi
75
96
22
4
Extract A 19 parts, sheep serum i part
60
...
61
35
*5
II
>9
11
0
5
Extract B
41
4
0
V
6
Extract B + o*i% glucose
61
60
...
75
85
9 >
84
104
3
7
Extract B i part, sheep scrum i part ...
-62*
5 ^
68
61
82
96
88
I
8
Extract B 19 parts, sheep serum i part
1
45
' 45
27
15
12
4
0
...
9
Extract C
47
5
0
...
10
Extract C -f- o*i% glucose
69
74
...
i 59
7 *
64
62
80
4
n
Extract C i part, sheep serum i part ...
66
58
7<5
70
70
89
126
I
12
Extract C 19 parts, sheep serum i part
59
...
49
30
22
>
3
0
...
13
Saline i part, sheep serum i part
78
...
...
71
86
70
no
114
52
H
Sheep serum
S8
86
93
89
102
72
* Average count of 6 tubes taken at random.
Considering, as a whole, the results obtained from the various
combinations of ‘ Extracted ' and normal serum, there appears to be
substantial ground for believing that the prolonged sojourn of
numerous trypanosomes in serum has isome effect on its capacity to.
support the parasites beyond that resulting from the mere removal
of glucose, and that this additional action is probably the result of the
removal of some other nutrient material rather than the production of
toxic substances. We have no knowledge of the nature of this
additional substance, which is of importance to the life of trypano-
somes, but the comparative failure of various modifications of
Ringer's solution to support trypanosomes (Tables V and VI), to
which reference will shortly be made, suggests that it is of the
nature of protein.
Summing up our observations on this subject, we have reached
the conclusion that the primary cause of the rapid death of the
trypanosomes in concentrated suspensions is the exhaustion of the
glucose content of the serum. Probably, however, other factors,
e.g., the exhaustion of other essential constituents of the serum and
possibly the excretion of auto-toxins by the parasites themselves,
play a secondary role in the phenomenon. It must, moreover, be
remembered in this connection that pronounced agglomeration of the
parasites into large masses is an invariable occurrence in concentrated
suspensions ; and as such masses rapidly subside to the bottom of the
tubes, the accumulation of the vast majority of the parasites into a
relatively small portion of the nutrient medium doubtless facilitates
the operation of these inimical factors. We have frequently observed
that when the clumping of the parasites into large agglomerations is
prevented and the trypanosomes maintained in even suspension by
frequent agitation of the medium, their length of life is considerably
prolonged.
The result of this work has consequently shown that, provided
the initial concentration of trypanosomes in the rabbit, or sheep,
serum does not exceed about i,ooo per c.mm., i.e., between 6o and 70
per 256 squares of the haemocytometer scale, the parasites survive in
practically undiminished numbers for a period of 24 hours at 37® C.
After this period, the number gradually falls, but if precautions are
taken to exclude bacteria, living parasites capable of infecting
mice may frequently persist in considerable numbers for three or four
days. It was subsequently found that the serum — fresh, or de-
activated at 56® C. for half an hour — of ox, horse, and pig, proved
just as efficacious as that of rabbit or sheep.
In striking contrast normal hixman serum was found to possess
SH
definite trypanocidal action. T. rhodesien$e and T. equiptrdum are
rapidly kiUed by human serum even in high dilutions, at 37° C. ;
but r. gdmbiense is apparently uninfluenced by human serum under
similar conditions. This action of human serum is so striking and
seems to have so important a bearing on the question of the
epidemiology of human trypanosomiasis that we have decided to
reserve further discussion of the matter to a separate paper.
Having reached this position as regards serum as a medium
for maintaining trypanosomes alive at 37® C., attention was turned
to other possible media. Experiments of a similar nature with
saline, various modifications of Ringer's* solution, nutrient broth,
and broth containing 0-2 per cent, glucose, showed that, in the absence
of serum, none of these are capable of supporting the parasites for
more than ja few hours at 37° C. (Tables V and VI). These tables
also illustrate the truth of our previous contention that when trypano-
somes, in suitable concentration, are suspended in sejrum, there is,
during the first 6 hours at least, a steady multiplication of the
parasites, and that after 24 hours, they are to be found in numbers at
least equal to those at the commencement of the experiment.
Apparently dilution of serum with Ringer-glucose solutions, to the
moderate extent shown in the tables, in no way impairs its capacity
to support the parasites.
Why, after the initial increase, there should be a continual
decline in the number of parasites until, after periods varying
from 48 hours to 96 hours or more, all are dead, and why this process
is more rapid in certain tubes than in others containing the same
medium we are unable to explain. One factor which certainly
is highly inimical to the life of the trypanosomes is bacterial
contamination, and this is difficult to eliminate entirely fcom
experiments of this kind. However, these questions are outside
the scope of the problem we set ourselves — the discovery of a
method whereby trypanosomes could be kept alive in undiminished
numbers over a period of at least 24 hours at 37° C. We are satisfied
that we have succeeded in finding a solution to this problem, and
• The constitution of the Ringcr^s solution was : —
Sodium chloride, 0*9 gm.
Potassium chloride, 0*025
Calcium chloride, ©*02 gm. - .
Sodium bicarbonate, 0*015 gm.
Pistilled water, 100*0 c.c.
Tapli: V.
Trypanosoma rhodesieme
Tube
Medium
Number of living trypanosomes per 2^6 squares
of the hacmocytometcr scale
Start
14
hours
3
hours
5
hours
6
hours
23
hours
3 ®
hours
48
hours
I
Physiological saline
I
1
0
2
Physiological saline + 0-2% glucose
1
j 10
3
0
3
Ringer’s solution
0
-
...
4
Ringer’s solution -f- o*i% glucose
20
:
2
0
5
Ringer’s solution -j- 0*2% glucose
24
22
8
2
6
Ringer’s solution -f 0*5 %glucose
27
21
15
2
...
7
Nutrient broth
28
21
5
...
8
Nutrient broth + 0*2% glucose
20
r>
...
9
Rabbit serum deactivated
3 *
1 •**
.35
24
•4
6
10
Rabbit serum deactivated om% glucose
45
3 *
21
3
ii
Rabbit serum deactivated 0*2% glucose
.29*
44
37
»4
i
12
Rabbit serum 2 parts Ringer 0*2% glucose i part...
4 ’ 1
26
13
I
«3
Rabbit serum i part -f Ringer 0*2% glucose 2 parts
39
,r. j
0
H
Rabbit scrum 2 parts -f Ringer glucose 1 part...
1
1
4 «
29
is ;
2
15
Rabbit serum i part + Ringer 0*5^^^ glucose 2 parts...
39
41
20 1
0
16
Sheep serum deactivated
35
40
29
25
9
*7
Sheep serum deactivated -f o*i% glucose
34
32
22
9
18
Sheep serum deactivated -f 0*2% glucose
42
27
'7
8
19
Sheep serum 2 parts -f Ringer 0*2% glucose i part ...
44
45
43 ,
34
20
Sheep serum i part + Ringer 0*2% glucose 2 parts ...
47
59
43
26
21
Sheep serum 2 parts -f Ringer o*5-{- glucose i part ...
36
30
12
1 [
22
Sheep serum 1 part -f Ringer 0*5% glucose 2 parts ...
j
47
i
40
]
37 '
34
* ThU figure U an average of the counts on 6 tubes taken at random.
Table< VL
Trypanosoma equiperdum
Number of living trypanosomes per 256 squares of
the haemocytometer scale
Tube
14
3
5
6
8
20
30
48
Start
hours
hours
hours
hours
I
0
hours
hours
hours
1
Physiological saline
0
...
...
...
...
1
Physiological saline -f o‘2% glucose
33
16
5
I
0
...
3
Ringer’s solution
0
...
...
...
...
4
Ringer’s solution -f o*i% glucose
33
«5
II
5
4
0
5
Ringer’s solution -f 0*2% glucose
42
21
*3
5
0
6
Ringer’s solution -\- 0-5% glucose
28
32
22
9
2
0
...
...
7
Nutrient broth
33
30
18
4 ,
I
0
8
Nutrient broth + 0*2% glucose
24
26
>9
9
0
...
9
Rabbit serum deactivated
35
58
...
4 ^>
>9
5
10
Rabbit serum deactivated -|- 0'i% glucose ...
40
50
39
24
II
1 1
Rabbit serum deactivated -f- 0-2% glucose ...
Rabbit scrum 2 parts Ringer 0*2% glucose
• 37 *
35
64
...
32
22
II
12
j part
44
74
62
29
I
»3
Rabbit serum i part -{- Ringer 0 ‘ 2 ‘^b glucose
2 parts
37
5 «
54
2
14
Rabbit serum 2 parts -f Ringer 0*5*?^ glucose
I part
64
52
34
5
15
Rabbit serum i part -|- Ringer o•f^^ glucose
2 parts
68
57
28 1
I
i6 '
Sheep serum deactivated
52
43
31
10
i
>7
Sheep serum deactivated -j- 1% glucose ...:
1
56
33
28
6
i8
Sheep serum deactivated + 0-2% glucose
...
...
53
44
26
II
>9
Sheep serum 2 parts -{- Ringer 0*2% glucose
1 part
47
45
32
9
20
Sheep serum i part -}* Ringer 0-2% glucose
58 i
2 parts
4 *
31
7
21
Sheep serum 2 parts -f Ringer 0-5% glucose
1 part
37
■ 52
10
22
Sheep scrum i part -f Ringer glucose
2 parts
... ^ 1
i ...
38
»3
* This figure is an average of counts on 6 tubes taken at random.
that the method will fulfil our requirements in that it will enable us
to examine the trypanocidal action of drugs and otlier substances
in vitro.
SUMMARY
1. As a preliminary step in an investigation of the mechanism
of the action of drugs in experimental trypanosomiasis, it appeared
desirable to study the action of the drugs in question in intro .
2. For this purpose it was obviously necessary to discover
some means whereby pathogenic trypanosomes could be preserved
alive in vitro ^ in approximately undiminished numbers, at 37° C. over
a period of at least 24 hours.
3. The efforts of previous investigators in this direction had not
met with much success. It was, however, generally agreed that
serum was the best medium, and that it was much easier to keep
the parasites alive at laboratory temperature than at 37® C. It is
not possible to obtain from this work information having any pretence
to quantitative value, and so far as work at the body temperature
is concerned, the only statement we have been able to discover of any
real value is that of Rothermundt and Dale (1912), who merely
recorded that in guinea-pig serum they were able to keep trypano-
somes alive for at least 5 hours ; the important question whether
the number of parasites decreased substantially during tliis period,
or whether the parasites were present in the same number at tlie
end of the period as at the beginning is ignored.
4. Our own experimental work showed that it is possible to
maintain a trypanosome suspension alive in vitro at 37° C., without
any appreciable diminution in the number of individuals, during
at least the first 24 hours.
5. The method of preparing such suspensions and of observing
changes in the number of parasites occurring in them, from time
to time, is described.
6. It is shown that serum — fresh, or deactivated at 56° C. for
half an hour — from the rabbit, ox, sheep, horse or pig, are about
equally efficacious as supporting media, and that physiological saline,
Ringer's solution — ^with or without the addition of glucose — nutrient
broth and broth containing 0*2 per cent, glucose are comparatively
useless.
518
7- Normal human serum, even in high dilutions, was found
rapidly to destroy rhodesieme and J. equiperdum at 37°C. in vitro ;
it had, however, no trypanocidal action on T, gambiense,
8. It was further shown that the concentration of trypanosomes
in the medium is a matter of vital importance. The parasites live
longest provided their concentration does not exceed about i,ooo
per c.mm. ; if they are present in concentrations grossly exceeding
this number, they die rapidly. The explanation of this fact is,
doubtless, bound up with the great metabolic activity of the trypano-
somes which, when the parasites are present in considerable
concentration, rapidly deprives the medium of its nutrient properties
and particularly of its glucose.
9. The presence of glucose is essential for the life of trypano-
somes in vitro. Information is supplied concerning the relatively
enormous quantity of glucose consumed by these parasites. It was
found that 0*25 c.c. of heavily-infected blood mouse, containing
approximately 400 million parasites, sufficed, when suspended in
5 c.c. of sheep serum, to which glucose had been added, to cause
within I hour the disappearance of between 2 mgm. and
2*5 mgm. of sugar, and within 5 hours of between 12 mgm.
and 12*5 mgm.
REFERENCES
Riot, C., Biot, R., .and Richard, G. (1911). Influence du Glucose sur la Vitality du Trypanosoma
hicisi in vitro. C.R. Soc. Biol., 71 , 368-69.
Kligler, I. J., and Wettzman, I. (1925). The Mode of Action of ‘ Bayer 205 * on Trypanosomes.
Ann. Trop. Med. & Parasitol., 19 , 235-41.
Nauss, R. W., and Yorke, W. (1911). Reducing Action of Trypanosomes on Haemoglobin. Attn.
Trop. Med. & Parasitol., 6, 199-2 14.
Papamarku, P. (1927). Versuche ueber die Wirkung chemotherapeutischer Stoife (Salvarsan,
Trypaflavin iind Antimonverbindungen) auf Spirochaten und Trypanosomen in vitro. Zeit.f,
Hyg. u. Infektionskr., 197 , 407-15.
Rothermvndt, M., and Dale, J. (1912). Experimentelle Studien uber die Wirkungsweise dcs
Atoxyls in intro und im Tierkdrper. Zeitscbr.f. Imm. u. exp. Tberapie., Orig. 19 , 565-94.
ScHERN, K. (1925). Ueber Trypanosomen. I-VI : Mitteilungen, Cent.-f. JBakt. I. Orig., 89 , 356,
360, 362, 440, 444, 451.
Terry, B. T. (191 1). The Advantages for Certain Experiments in vitro of suspending Trypanosomes
in Serum. Proc. Soe, Exp* Biol* & Med,, 9 , 40-41.
(1915). The Influence that Scr^ exerts, upon Trypanosomes, with Special Reference to
its Use for Experiments in vitro with Atoxyl and Paraminophenylarsenoxyd. Jl. Exp. Med.,
21, 250-57.
STUMPY AND POSTERIOR-NUCLEAR
FORMS IN A STRAIN (FEROX) OF
TRYPANOSOMA B RUG El
BY
GEORGE MACLEAN,
SL££P1NG SICKNESS OFFICER, TANGANYIKA TERRITORY
[From the Pathological Department of the University and Western
Infirmary, Glasgow)
[Received for publication 4 November, 1929)
There has long been considerable doubt about the relationship
between the Trypanosoma brucei originally described by Plimmer
and Bradford in 1899 and maintained in European laboratories
since, and the polymorpliic 7 \ brucei or ugandae now met with in
the field. Bruce had discovered a trypanosome in domestic stock
suffering from nagana in 1895, and the figure of this parasite which
he gave in 1897 showed it to be polymorphic. In 1899 trypanosomes,
considered to be the same as that figured in 1897, were investigated
in England by Plimmer and Bradford and named T. brucei.
According to their description the trypanosome was monomorphic.
Stephens and Fantham also described their strain, derived from
that of Plimmer and Bradford, as monomorphic. Presumably the
various laboratory strains of T. brucei have come from this original
infection.
Differences in their immunity reactions described by Kroo
and by Browning and Gulbransen are no doubt to be ascribed
to the fact that the strains have been passed through different
animal hosts at various times, and the infections have not been
restricted to mice. At the early period of investigation on trypano-
somes little attention was paid to such points as the influence of
the host on the parasites, which may be very enduring. This first
appeared from the work by Ehrlich, Roehl and Gulbransen
on serum-fast strains.
It may therefore be of interest from the morphological point
of view to record that in a ‘ ferox * strain of 1 \ brucei* received
from Professor Mesnil, Institut Pasteur, Paris, in a guinea-pig
sixteen months ago and since kept in mice at the Pathology Depart
ment, Glasgow University, the writer observed on several occasions
* This strain was obtained through the Medical Research Council.
519
520
stumpy forms. Among these there were six individuals showing
various degrees of posterior nuclear displacement, one being a typical
‘ posterior-nuclear ' form.
This typical posterior-nuclear individual was seen in the blood
of a mouse in which the parasites were gradually disappearing as
a result of the administration, 42! hours previously, of the anil
preparation No. 71 (Browning, Cohen, Ellingworth and Gulbransen).
It had no free flagellum and the nucleus was displaced almost
completely to the posterior end. The cytoplasm did not show
the granular appearance sometimes seen after drug treatment.
The other five were seen in the blood of a mouse which had
been treated 45 hours before wdth the styryl preparation No. 90.
Four of these were dividing forms, two nuclei being present,
while the cytoplasm was still unsegmented. In these one nucleus
was placed centrally while the other was almost or completely within
the j>osterior quarter, that most displaced being about half its
own diameter from the posterior end. The remaining specimen
sliowed no signs of division ; its nucleus was partly within the
posterior quarter and was separated by a little more than its
own length from the posterior end of the trypanosome. Though
the axoneme was quite distinct there was little or nothing
of the flagellum free. I'he cytoplasm showed coarse granules
scattered throughout it.* In some of the other stumpy forms
there were marked granular changes and neither axoneme nor
undulating membrane could be seen, but in at least four specirhens
(one before and three after treatment) the axoneme was quite
distinct though there was no free flagellum.
Altogether over 10,000 trypanosomes were examined.
REFERENCES
Bkownino, C. H., Cohen, J. B., Ellingworth, S., and Gulbransen, R. (icjiO), IVoc, lioj', 6'oc\, li.f
ido, 293.
{ 1929 ), Ibid., 105 , 99.
and Gulbransen, R., see Browning, C. H. (1927), Brit. Med. yourn., 2 , 1405,
Ehrlich, P., Roeiil, W., and Gulbransen, R. (1909), Ztscbr.f. Immunitatsforsch., 3 , 296.
Kroo, n., 1926, Ztsebr. /. Hyg. u. Infkr., 106 , 77.
Wenyon, C. M., ‘ Protozoology,* London, 1926, gives full references to the earlier literature.
• The animal# from which the specimens were obtained were killed several days later when the
parasites, as judged by microscopical examination, hatih^isappeared from the blood, thus the further
course of the infections could not be determined.
AEDES {AEDIMORPHUS) APICO-
ANNULATUS EDWARDS AND YELLOW
FEVER : A CORRECTION
BY
A. M. EVANS
{Received for publication 22 November, 1929)
In our recent work, ' Insects, Ticks, Mites and Venomous Animals
of Medical and Veterinary Importance,* Professor Patton and the
present writer refer, on page 198, to Bauer’s (1928) transmission
of Yellow Fever by A, (AMimorphtis) apicoannulatus Edwards.
It now appears certain, however, from an examination of specimens
kindly presented to the Liverpool School of Tropical Medicine by
Mr. C, B. Philip, of the West African Yellow Fever Commission,
that the species referred to by Bauer was not apicoannulatns, but a
somewhat similar species, which I found to be quite distinct from
Edward*s species, when working in Sierra Leone, where both species
occur. This species, which I named occidentalis (1926), was
uncommon in Freetown, in comparison with apicoannulatus, but
material identified by other workers from Nigeria and the Gold
Coast, has invariably been found to be, in reality, occidentalis.
Further, Mr. Edwards informs me that he has not seen apicoannulatus
from Nigeria or the Gold Coast.
As the synonomy given below will show, these two species have
been confused in the literature since 1917 and the paper, in which I
distinguished occidentalis, has evidently been overlooked by recent
workers. In this paper I described the larva of apicoannulatus,
and pointed out that Ingram and Maefie’s description, based on their
Gold Coast material, applies to the larva of occidentalis, as I found
by rearing such larvae to the adult state in Freetown. It should be
noted that, in the table showing the larval differences on page 102
of my paper, the names of the twa species are reversed.
The chief difference between these two species, as is noted in our
book (1929), is the possession by occidentalis of conspicuous paired
522
patdies of white scales on the* lantero-lateral margins of ^he
mesonotnm. Another obvious difference is the total absence of a
pale band on the proboscis, the possession of such a band being a
conspicuous feature of apicoanntdatu$, as shown in our figure on
p. 289. The ^ hypopygium also shows very marked differences,
as shown in my paper {1926).
While this paper was in the press I discovered that the name
occidentalis is preoccupied in the genus Aedes by an Australian species
of vSkuse, so that a new name will have to be given to the West
African species. It is proposed, therefore, to rename it AMes
{Aedimorphus) stokesi in honour of Dr. Adrian Stokes, who died of
Yellow Fever while working with Dr. Bauer and Dr. Hudson on the
experiinental transmission of this disease to laboratory animals.
The Synonomy of these species is now as follows : —
Aede$ (Aedimorphus) opicoafino/afas Edwards (1912). Bull, Ent. Res.
Aedimorphus alboannulatus Theobald (1905).
Aedes (Aedimorphus) stokesi nom. nov.
Aedes (AMimorphus) occidentalis Evans (1926). Ann. Trap.
Med, and Parasitol,
Aedes {AHimorphus) apicoannulatus Edwards (1923).
Aedes {Aedimorphus) apicoannulatus Edwards {1925).
Ochlcrotatus apicoannulatus Ingram and Macfie (1917).
Aedes {Aedimorphus) apicoannulatus Bauer (1928).
REFERENCES
Bauch, J. II. (1928). The transmission of Yellow Fever by mosquitoes other than Aedes aegypti.
Am. Jl. Trap. Med.., 8 , 261.
Edwards, F. W. (1925). Mosquito Notes, V. Bull. Ent. Res.y 15 , 257.
Evans, A. M. (1926). Notes on Freetown mosquitos, with descriptions of new and little-known
species. Attn. Trop. Med. & Parasitol.^ 20 ) 97-
Ingram, A., and Macfie, J. W. S. (1917). The early stages of certain West African mosquitoes.
Bull. Ent. Res., 8 , 135.
Patton, W. S., and Evans, A^ M. (1929). Insects, ticks, mitCs and* venomous animah of medical
and veterinary importance. Part I ; Medical. Liverpool,* 8vo. Published by I^rofesior
Patton, pp. i-xi ; 1-786, 60 Plates, 374 Text-figs.
PATHOGENICITY OF TRYPANOSOMA
LEIFISI AND BLOOD SUGAR IN
INFECTIONS WITH TRYPANOSOMA
LEWISI AND BARTONELLA MURIS
RATTI
BY
PAUL REGENDANZ
{Insiitid filr Schiffs-tmd Tropenkrankheiten- Hamburg, Department
of Protozoology)
{Received for publication 9 September, 1929)
A short time ago it was published by Linton (1929), in these
Annals, that generally, in accord with our own experiences, he had
found that the blood sugar level of normal and splenectomized rats
was not lowered by infections with normal and non-lethal strains of
T, lewisi. We have, however, experimented also with a strain of
T. lezoisi which had become virulent to such an extent, that it often
produced a fatal infection in splenectomized rats. In such cases
we have always found a final hypoglycaemia. The opinion of Linton
is that the death of these animals was not caused by the infection
with T. lewisi, but by an infection with Bartonella, which was
responsible for the depressed sugar level.
He states, further, that it is very difficult to avoid infection
with Bartonella in experiments with T. lewisi in splenectoniised rats.
But this is not quite exact. As ascertained by Mayer, Borchardt
and Kikuth, the organic arsenicals, i.e., Neo-Salvarsan, Atoxyl,
Tryparsamide, etc., are of high therapeutic value against Bartonella
nturis ratti. These drugs are, however, entirely ineffective against
T. lewisi. There is at present only one drug, i.e., Arsenophenylglycin,
to which T. lewisi is susceptible and by which it can be destroyed
when employed in doses as indicated below. The opinion of
Taliaferro (mentioned by Stratman-Thomas and Loevenhart (1928),
that Arsenophenylglycin is not active against T. lewisi can only be
explained by supposing that the preparations he used were not
523
identical with the ones employed by us {kindly placed at our disposal
by the I. G. Farbenindustrie-Elberfeld). Reichenow and Regendanz,
and Kikuth and Regendanz, have for several years employed this
drug for experiments with T. lewisi and found it extremely efficacious
even with doses of 0*10 grams to 0*17 grams per kilo body-weight.
It is, therefore, easily possible to work with splenectomised rats in
experiments of infections with T. lewisi as the infection with
Bartonella can be eliminated by, say, Neo-Salvarsan, which does not
influence T, lewisi.
In the work of Regendanz and Tropp, we have not called special
attention to the fact, that the splenectomised rats have been treated
with Neo-Salvarsan beforehand, for at the time we were making a
statement on the sugar metabolism in Trypanosomiasis. But in a
paper published at the same time by Regendanz and Kikuth, we
mentioned this fact. Besides, we have always examined prepara-
tions of rat blood stained with Giemsa's solution, so that infections
with Bartonella could not be overlooked.
The question whether T. lewisi can produce fatal infections in
the rat, has kept turning up for years. Several experimenters
who have been studying this form of trypanosomiasis intensively,
have observed an occasional occurrence of pathogenic action. We
need not go into the existing literature on the subject, which is
well known. The strain of T, Uwisi, with which we worked, had
become so virulent by quick successive inoculations and cultivations
in N-N-N-Agar, that even a non-splenectomised rat died of infection
with this strain, as described by Reichenow and Regendanz. In
the blood of this rat were dividing forms for eight days prior to its
death, while normally the period of division is very much shorter.
But it must also be observed, that even in non-splenectomised
rats an infection with T. lewisi may activate an infection of Bartonella.
Mayer observed in a normal rat infected with T. lewisi the
spontaneous appearance of Bartonella, having already (1921) dis-
covered Bartonella muris ratti in chemotherapeutical experiments in
normal rats infected with pathogenic Trypanosoma (T. rhodes). We,
too, observed the occurrence of a strong infection with Bartonella
in a non-splenectomised rat as the result of an infection with T. lewisi.
As the spleen forms protective substances against Bartonella infection
in rats, as shown by Mayer, Borchardt and Kikuth, as well as against
infection with T. Icwisi, as shown by Regendanz and Kikuth, the
activation of Bartonella infection is thus brought about by the fact
that the spleen, taken up with the production of antibodies against
T. lewisi, fails to cope with the Bartonella infection.
We have now examined the blood sugar of rats infected with
Bartonella. The rats were splenectomised and after the blood had
been strongly infected with Bartonella, we made the determination
of blood sugar. The blood was obtained by decapitation and the
glucose determined after Hagedorn- Jensen.
Taule I.
Rats
number
Days
Blood sugar
in mgs. per
100 c.cms.
I
2
3
5
6
I
Splenectomy...
0
0
0
f
•1'
Sacrificed. Not fed for 20 hours.
108
2
0
c
0
4
4 '
Sacrificed. Not fed for 20 hours.
109
3
0
0
0
■]
Sacrificed. |
I
U 9
4
0
c
1-
4 -
Died spontaneously.
7 »
5
V,
u
u
0
-f-
1 1
Died spontaneously. Nut fed
for 22 hours.
20
-j- - Bartonella in the blood.
As shown in the table, we only found a depression of the blood
sugar level in animals which had died of infection with Bartonella
(Rats 4 and 5). The examinations could be made immediately after
the death of these rats. A depression of blood sugar did not exist
in the three other rats infected with Bartonella (Rats i, 2 and 3).
Our results herein correspond with those of Linton.
It must still be considered that, as Regendanz observed in
Trypanosomiasis of large animals such as monkeys, there is a
disturbance of the blood sugar metabolism during the course of the
infection. That does not generally happen with rats, perhaps
because in them the infection with trypanosoma takes too rapid a
course to allow the onset of disturbances of organs controlling the
glucose metabolism. Therefore, it may be that similar conditions
exist in infections of rats with Bartonella.
CONCLUSION
In rats dying of infections with Bartonella marts ratii there
occurs a final hypoglycaemia.
Trypanosoma lewisi may sometimes have a pathogenic action
on rats in which there is a final hypoglycaemia.
It is easy to eliminate the Bartonella infection in splenectomised
rats infected with lewisi by arsenical preparations, without
influencing these latter parasites, as Bartonella and T. lewisi react
differently to all known organic arsenicals except Arsenophenylglycin.
REFERENCES
Hacedorn, H. C., and Jensen, Norman B. (1923). Zur Mikrobcstimmimg dcs Blutzuckcrs mlttels
I'errizyanici, Blochem. Zuhr.^ 135 , 46.
Kikuhi, W.. and Rf.gendanz, P. (1929). Ueber die Beziehungen der cheinothcrapfutischen Millcl
zum ‘ Rcticulocndothel.’ Zschr.f. Jmmunitat^forsih.^ 61 , 422.
I.iN'iON, Richard W. (1929). Blood sugar in infections with Trypanosoma h'tvisi. Ann. T rop. Mid.
and Parasitol.^ 23 , 307.
jMaykk, JM. (1921). Ueber cinige baktcrieniihniichc Ihirasiten dcr Erytlirozytcn bci Menschen und
'Picren. Arch. f. Schiffs-n. Tropenbyg..^ 25 , 150.
Houchardt, W., and Kikhth, W. (1927). Die durch Milzcxstirpation auslosbare
infektiosc Rattcnanacmic. Arch. f. Schijfs.-u. Tropenhyg.. 31 , Beihcft 4.
Regendanz, (1929). Der Blutzuckcr bci Trvpanosomeninfektionen. Arch. f. Schif}s.~n,
Tropenhyg.^ 33 , 242.
and Kikuth, W. (1927). Die Bedeutung der Mllz fur die Bildung dcs vermchrungs-
hindernden Rcaktionsproduktes (Taliaferro) und dessen Wirkung auf den Infcktionsvcrlaiif
der Ratten-Trypanosomiasis (Tryp. Icudsi). Ctrbl. f. Bakf.., 103 , 271.
and Tropp, C. (1927). Das Vcrhalten dcs Blutzuckcrs und des Lcbcrglykogcns bei
mil Trypanosomcn infizicrtcn Ratten. Arch.f. SchiJ^s.-n. Tropenhyg..^ 31 , 376.
Reichenow, E., and Regendanz, P. (1927). Ueber die Flohpassagc normaler und mit Arseno-
phenylglycin vorbehandclter Rattentrypanosomen. Abb. a. d. Gebiet d. Anslandskundc.,
Hamburg. IJniversitdt. 26 , Reihe D. Medizin, 2 {Fctsschrift Nocht), 446.
Stratman-Thomas, W. K., and Loevenhart, A. S. (1928). 'I'he therapeutic value of Etharsanol
and Proparsanol in experimental Trypanosomiasis of rats and rabbits, yi. Pharm. &' Exp.
Therap..^ 33 , 459.
INDEX
INDEX
fACE
Index of Authors iii
General Index iii
Index of Genera, Species and Varieties new to Science vii
INDEX OF AUTHORS
PAGE
Adams, A. R. D. ; Yorke, Warrington ;
and Murgatroyd, F 501
Adler, S.; and Theodor, 0 1,19, 269
Comaroff, R., and Kligler, L J 103
Comaroff, R.; Kligler, I. }., and
Geiger, A 325
Datta, M. N., and Verma, S. C 483
Evans, A. hi 407, 415, 521
Geiger, A.; Kligler, I. J., and
Comaroff, R 325
Gray, J. D. Allan 241
Hilmy, I. S 385
Hilmy, I. S., and Southwell, T 381, 397
Huff, Clay G 427
KUgler, I.J 315
Kligler, I, and Comaroff, R 103
Kligler, I. J.; Geiger, A., and
Comaroff, R 325
T.inton, R. W 307
GENERAL
page !
Acanthosentis n.gen., from a Calcutta Fish 483 |
„ antsfinusTi.^^ 484 j
Acoleidae 404 0
Adams, A. R. D.; Yorke, Warrington, j
and Murgatroyd, F. Studies in Chemo- j
therapy. I. — ^A Method for Main- |
taining Pathogenic Trypanosomes alive i
In Vitro at 37° C. for 24 hours 501
Adler, S., and Theodor, O. Attempts to 1
transmit Leishmania tropica by Bite ;
the Transmission of L. tropica by Phle-
hotomus sergenti i
Adler, S., and Theodor, O. The
Distribution of Sandflies and Leish-
maniasis in Palestine, Syria and
Mesopotamia 269
iii
PAGE
Maclean, George 37, 337, 345, 519
Magath, Thomas B 121
Mitchell, J. A 443
Murgatroyd, F.; Yorke, Warrington,
and Adams, A. R. D 501
Nagaty, H. F 349
Fillers, A. W. N., and Southwell, T. 129, 130
Regendanz, P 523
Sandground, J. H 23
Southwell, T 47
Southwell, T., and Hilmy, I. S 381, 397
Southwell, T., and Fillers, A. W. N. 129, 130
Stephens, J. W. W 45 1
Taylor, A. W 33
Theodor, 0 ., and Adler, S i, 19, 269
Verma, S. C., and Datta, M. N 483
Witenberg, G 1 3 1
Yorke, Warrington ; Adams, A. R. D.,
and Murgatroyd, F 501
INDEX
PAGE
Adler, S., and Theodor, 0 . Additional
Evidence on the Occurrence of
L. tropica in wild Phlebotomus papatasii 19
Adleria n.gen 143, 206
„ minutissima 143,206
Adleriinae n.mhi 143,206
Aedes{Aedmorphus) apicoannulatus Edward 521
„ ,, stokesi nom, nov. ... 521
Africa, Blackwater Fever in 67
America, North, Blackwater Fever in ... 451
Anopheles marsh alii var. Jreetozvnensis
Evans ... 422
„ „ „ hargreavesi
Evans , . . 420
„ „ „ moucheti
Evans ... 413
PAGE
ApophdUus Liihe, 1909 183
Aviullinky Genus and Species 349
„ aegyptiaca n.sp 3^
„ centripunciata (Rivolta), 1874,
Railliet, 1893 359
„ souihwelli n.sp 364
„ Woodland, 1927 362
Avitellininae 47
Bartonella muris ratti and Blood Sugar ... 523
Bayer 205 in Rhodesian Sleeping Sickness 337
Blackwater Fever in Africa 67
„ „ „ North America 451
Bothriocephalus scorpii (Mueller, 1776)
Cooper, 1917 385
Centrocestinae Looss, 1899 184
Cercarioides n.gen 142, 197
„ aharonii n.sp 142, 198
Cercarioidinae 142, 197
Comaroff, R., and Kljgler, I. J. Suscepti-
bility and Resistance to Trypanosome
Infections. V. — The Resistance of
Rats to Infection 103
Comaroff, R.; Kligler, I. J., and Geiger, A.
Susceptibility and Resistance to Try-
panosome Infections. VII. — Cause of
Injury and Death in Trypanosome
Infected Rats 325
Crepidobothrium testudo (Magath, 1924)... 121
Crithidial Infections in Phlehotomus
minutus var. afriranvs 33
Cryptorotyle 180
„ Liihe, 1899 180
Cryptocotylea n.tr 142, 180
Culex (Culiciomya) cinerellus Edw 41 1
„ pipiensj Susceptibility to Plasmod-
ium cathemerium 427
Datta, M. N., and Verma, S. C. Acantho-
cephala from Northern India. I. — A
New Genus A canthosentis from a
Calcutta Fish 483
Dexiogonimus n.gen 140, 170
„ ciureanus n.sp 140, 170
Diorchiirema n.gen 140, 173
„ pseudocirrata n.sp 140, 174
Diploposthidae 404
Evans, A. M. Descriptions of the Early
Stages of Two Further Mosquitos
Collected in Southern Nigeria by
Mr. L. H. Dunn 407
PAGE
Evans, A. M. Notes on Certain Varieties
of Anopheles marshalli Theobald 415
Evans, A. M. Aedes {Aedimorphtts)
apicoannulatus Edwards and Yellow
Fever : A Correction 521
Galactosomum Looss, 1899 179
Geiger, A.; Kligler, I. J., and Comaroff, R.
Susceptibility and Resistance to ^
Trypanosome Infections. VII. — Cause
of Injury and Death in Trypanosome
Infected Rats
•••
Gray, J. D. Allan. A Study of Experi-
mental Infection by treponema duttoni ;
with a Review of the Literature
... 241
Haplorchinae 1899) Poche, 1926... 200
Haplorchis Looss, 1899
.. 200
Harpagomvia jarquharsoni Edw
.. 407
Heterophxea n.tr
.. 140
Heierophyes
.. 144
„ aequalis Looss, 1902
.. 166
„ dispar Looss, 1902
.. 163
„ heterophyes
.. 149
„ Onji, 191S
.. 162
Heterophyidae, Bibliography
.. 209
„ Classification
••• 134
„ Life-Cycle
••• 133
„ Life-History
•• 143
Hilmy, 1 . S. Bothriocephalus scorpii
(Mueller, 1776) Cooper 1 91 7
... 385
Hilmy, 1 . S., and Southwell, On
a New Species of Phyllohothrhim
{P. microsomum) from an Indian Shark 381
Hilmy, I. S., and Southwell, T. Jardugia
paradoxa, a New Genus and Species of
Ccstode with Some Notes on the
Families Acoleidae and Diploposthidae 397
Huff, Clay G. The Effects of Selection
upon Susceptibility to Bird Malaria in
Culex pipiens Linn 427
Jardugia 397
„ paradoxa n.sp 397
Kligler, I. J. Susceptibility and Resistance
to Trypanosome Infections, VI. — The
Course of the Infection in Splenec-
tomized Rats 315
Kliger, 1 . J., and Comaroff, R. Suscepti-
bility and Resistance to Trypanosome
Infections. V. — The Resistance of Rats
to Infection 103
IV
PAGE
Kligler, I. J.; Geiger, A,, and Comaroff, R.
Susceptibility and Resistance to Try-
panosome Infections. VII. — Cause of
Injury and Death in Trypanosome
Infected Rats 325
Leiperia cincinalis Sam bon. Nymph of... 130
Leishmania tropica by Phlebotomus papa-
tasii, Exerimental
Transmission of ... 2
„ in Wild Phlebotomus
papatasii 19
„ by Phlebotomus ser-
genti, Experimental
Transmission of ... i
Linton, R. W. Blood Sugar in Infections
with Trypanosoma lewisi 307
Maclean, George. The Relationship
between Economic Development and
Rhodesian Sleeping Sickness in
Tanganyika Territory 37
Maclean, George. Notes on Treatment of
Fifty-two Cases of Rhodesian Sleeping
Sickness with Bayer 205 and Trypar-
samide 337
Maclean, George. The Action of
Prap. 3510 in Rhodesian Sleeping
Sickness 345
Maclean, George. Stumpy and Posterior-
Nuclear Forms in a Strain (Ferox) of
Trypanosoma brucei 519
Magath, Thomas B. The Early Life-
History of Crepidobothrium testudo
(Magath, 1924) 12 1
Metagonimus 169
Microlistrum Braun, 1901 179
Miscellanea 129
Mitchell, J. A. Tunnel Rat-Trap for
Stores and Ships 443
Monorchitrema Nishigorj, 1924 200
„ Nishigori, 1924... 201
„ taihui Nishigori, 1924 ... 203
Murgatroyd, F.; Yorke, Warrington, and
Adams, A. R. D. Studies in Chemo-
therapy. I. — A Method for Maintaining
Pathogenic Trypanosomes alive
In Vitro at 37° C. for 24 hours 501
Nagaty, H. F. An Account of the
Anatomy of Certain Cestodes belonging
to the Genera Stilesia and Avitellina... 349
Nematode Parasite, Infection with
Unidentified 23
PAGE
Nigeria, Northern, Phlebotomus minutus
var. africanus in 33
Parascocotyle ascolonga n.sp
194
„ italica (Alessandrini,
1906) 192
„ longa (Ransom, 1920)
189
„ Stunkard, 1924
187
Phlebotomus as carriers of Oriental Sore,
Species of
269
„ Distribution of Varieties of
in Palestine, Syria, and
Mesopotamia L 20, 269
Phlebotomus minutus var. africanus in
Northern Nigeria 33
„ papatasii in Experimental
Transmission of
„ „ Leishmania tropica 2
Wild, Infected with
Leishmania tropica 19
„ sergenti in Experimental
Transmission of Leishmania
tropica i
Phyllobothrium microsomum n.sp 381
Fillers, A. W. N., and Southwell, T.
Strongyloidosis of the Woolly Monkey
(Lagoihrix humholdti) 1 29
Fillers, A. W. N., and Southwell, T.
A Note on a Nymphal Linguatulid —
Leiperia cincinalis Sam bon — from the
Musculature of the Fish Tilapia nilotica 130
Plasmodium cathemcrium, Susceptibility of
Culex pipieiis to 427
Prap. 3510 in Rhodesian Sleeping Sickness 345
Pygidiopsis Looss, 1907 185
„ genata Looss, 1907 185
Rat-'Frap for Ships and Stores 443
Regendanz, P. Pathogenicity of Trypano-
soma lewisi and Blood Sugar in
Injections v/ith Trypanosoma lewisi and
Bartonella muris ratti 5^3
Rhodesia, Southern. Ternidens deminutus
(Railliet and Henry) in 23
Rhodesian Sleeping Sickness in Tanganyika -
Territory 37
Rhodesian Sleeping Sickness, Treatment
by Bayer
20i; and
Try pars a-
mide
337
Treatment
by Prap.
3510
345
V
PAGE
Rossu'otrma Skrjabiny. 1919 182
Sandflies, see Phlebotomus.
Sandground, j. H. femidens dmtnuius
(Railliei and Henry) as a Parasite of
Man in Southern Rhodesia ; together
with Observations and Experimental
Infection Studies on an Unidentified
Nematode Parasite of Man from this
Region 23
Southwell, T. Notes on the Anatomy of
Stilesia hefatica, and on the Genera of
the Sub-Family Thysnnosontittae (in-
cluding Avitellininae) 47
Southwell, T., and Hilmy, I. S. On
a New Species of Phyllohothrium
{P. mictosomum) from an Indian Shark 381
Southwell, T., and Hilmy, I. S. Jardugia
paradoxa^ a New Genus and Species of
Cestode with some Notes on the
Families Acoleidae and Diplopo'sthidae 397
Southwell, T,, and Fillers, A. W. N.
Strongyloidosis of the Woolly Monkey
{Lagothrix humboldii) 129
Southwell, T., and Fillers, A. W. N.
A Note on Nymphal Linguatulid —
Leiperia cincinalis Sambon — from the
Musculature of the Fish Pilapia nilotica 130
Stephens, J. W. W, The Distribution of
Blackwater Fever in Africa 67
Stephens, ]. W. W. The Distribution of
Blackwater Fever in North America ... 451
Stiftodora I.ooss, 1899 176
„ sawahinensis l^oss, 1899 176
Siilesia, Genus and Species 349
„ glohipimctaia (Rivolta), 1874,
Railliet, 1893 352
„ hepatica Wolffhvigel, 1903 358
„ hepatica 47
„ vittata, Railliet, 1896 355
Strongyloidosis in Woolly Monkey 1 29
Tanganyika Territory, Sleeping Sickness
in 37
Taylor, A. W. Notes on the Occurrence
of Crithidia in Phlebotomus minutus var.
africaniis in Northern Nigeria 33
Pernidens deminutus (Railliet and Henry) 23
PACE
Theodor, O., and Adler, S. Attempts to
transmit Leishmanta tropica by Bite ;
the Transmission of Z. tropica by
Phlebotomus sergenti i
Theodor, 0 ., and Adler, S. Additional
. Evidence on the Occurrence of
L. tropica in Wild Phlebotomus papatasii 19
Theodor, O., and Adler, S. The Distribu-
tion of Sandflies and Leishmaniasis in
Palestine, Syria, and Mesopotamia 269
Thysanosominae (including Avitellininae) 47
Tocotrema (Looss, 1899) l8i
Treponema duttoni, Experimental Infection
with 241
T rypanosoma brucei, Stumpy and Posterior-
Nuclear Forms in Strain of 519
Trypanosoma letvisi and Blood Sugar 523
Trypanosomes alive In Vitro ^ Method for
keeping 5^^
Trypanosome Infections, Susceptibility
and Resistance
to 103
„ Resistance of
Rats to 103
„ „ in Splenecto-
mized Rats 315
„ „ Cause of Injury
and Death in
Infected Rats 325
Trypanosoma letvisi, Blood Sugar in
Infections with 307
Tryparsamide in Rhodesian Sleeping
Sickness 337
Verma, S. C., and Datta, M. N. Acantho-
cephala from Northern India. I. — A
New Genus Acanthosentis from a
Calcutta Fish 483
Witenberg, G. Studies on the Trematode
— Family Heterophyidae 131
Yellow Fever and Aedes (Aedimorphus)
apicoannulatus Edwards 521
Yorke, Warrington ; Adams, A. R. D., and
Murgatroyd, F. Studies in Chemo-
therapy. I. — A Method for Maintaining
Pathogenic Trypanosomes alive
In Vitro at 37° C. for 24 hours 501
VI
INDEX OF GENERA, SPECIES AND VARIETIES NEW TO SCIENCE
PAGE
Acanthosentis n.gcn 483
„ antspinusTi.%^ 484
Adleria n.gen 143
„ minutissima n.sp 143
Adleriinae n.subf 143
Avitellina aegyptiaca n.sp ^66
„ southwelli n.sp 364
Cercarioides n.gen 142
„ aharonii n.sp 142
Cercarioidinae n.subf 142
PAGE
Crypiocotyka n.tr 142
Dexiogo?iimus n.gen 140
„ dure anus n.sp 140
Diorchitrema n.gen 140
„ pseudodrrata n.sp 140
Heterophyea n.tr 140
Jardugian.g 397
„ paradoxa n.sp 397
Parascocotyle ascolonga n.sp 142
Phyllohothriuni microsomum n.sp 381
I.A.R,1. 75
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